1. 动物社交倾向的界定与行为表现
1.1 内向-外向维度在动物中的类比与测量
在动物行为研究中，尽管内向-外向（Introversion-Extroversion, I/E）维度与人类I/E的内涵不尽相同，但其在量化动物社交倾向方面提供了重要的框架，被广泛用于描述个体在社交活动中的偏好和表现。这种类比主要通过一系列可观察的行为学指标来实现，旨在评估动物对社交互动的频率、强度以及参与意愿。
社交互动频率是衡量动物社交倾向的核心指标之一。例如，研究人员会记录动物在特定时间内与同类个体进行接触（如嗅探、追逐、理毛等）的次数，高频率的互动通常被视为外向倾向的体现。群体参与度则关注个体在群体活动中的融入程度，包括是否主动加入群体、在群体中的位置以及对群体行为的贡献等。陌生个体接触意愿则通过引入不熟悉的同类个体来评估动物的社交探索行为，例如在三箱实验（three-chamber test）中，小鼠会表现出与新奇同类而非熟悉同类或空笼子待在一起的偏好，这种偏好反映了其社交动机和对新奇社交刺激的兴趣 12。
为了更精确地量化这些行为指标，研究人员开发了多种行为分析工具和范式。例如，克劳利社交和新奇社交偏好协议（Crawley's sociability and preference for social novelty protocol）是小鼠社交行为研究中常用的三箱范式。该测试允许实验小鼠自由选择在三个隔间中的任意一个花费时间，其中一个隔间放置一个陌生同类，另一个隔间为空白或放置一个熟悉同类。通过测量小鼠与陌生同类相处的时间以及对陌生同类与熟悉同类的偏好，可以评估其社交亲和力、社交动机、社交记忆和新奇偏好等关键社交行为方面 1。这种方法提供了量化小鼠社交倾向的有效手段，并已成功应用于多种近交系和突变小鼠的研究中 1。
此外，更先进的技术，如高分辨率3D姿态追踪和社交接触分析，正在被应用于自由互动动物的社交行为研究，特别是在啮齿动物（如大鼠和小鼠）中。例如，有研究通过3D几何推理、图神经网络和半监督学习解决了主体遮挡和身体部位分配等挑战，成功追踪了交互动物的姿态动态和社交接触 3。这种方法能够识别出一系列刻板的动作、互动、同步性和身体接触，为社交行为的精细表型分析提供了可能，尤其是在自闭症模型动物中，这种高分辨率的表型分析揭示了传统测量方法无法解析的变化 3。通过这些先进的工具，研究人员得以从微观层面理解动物社交倾向的复杂结构和潜在机制。
1.2 不同物种的社交倾向典型表现
动物的社交倾向在不同物种间表现出显著的多样性，这反映了它们在特定生态环境和进化压力下的适应性策略。通过对比不同动物类群的社交行为，我们可以更好地理解“内向”和“外向”在动物世界中的具体表现。
灵长类动物：灵长类动物通常表现出高度复杂的社交结构和外向的社交倾向，这在它们的合作觅食、社会等级建立和育幼行为中尤为明显。例如，许多灵长类物种会形成稳定的群体，个体之间通过复杂的交流（如理毛、叫声、面部表情）维持社会联系。在合作觅食方面，一些灵长类物种展现出高度协调的行为，共同搜寻食物、分享资源，甚至进行群体防御以保护食物来源或幼崽。这种合作行为不仅增加了觅食效率，也强化了群体内部的凝聚力，是其外向社交倾向的重要体现。此外，动物的复杂社会行为需要多种认知技能，包括个体识别和观察学习，这些技能是社会系统进化的基础 4。
啮齿类动物：啮齿类动物的社交行为模式多样，既有高度社会化的物种，也有相对独居的类型。例如，大鼠被发现具有显著的亲社会行为。在一项经典实验中，一只自由活动的大鼠会学习如何打开限制器来解救被困的同伴，即使这并不直接为自己带来益处。当同时提供巧克力奖励时，大鼠通常会打开两个限制器并分享巧克力，这强有力地证明了它们对同类困境的同情心和亲社会动机 56。这种互助行为体现了其一定程度的外向社交倾向，尤其是在面对同伴困境时。草原田鼠（prairie voles）则以其严格的一夫一妻制和高度的伴侣偏好而闻名，它们会形成稳定的配对关系并共同育幼，催产素在这种伴侣关系形成中扮演关键角色 7。
鸟类：鸟类的社交行为同样丰富多彩，包括混合物种群的形成、合作繁殖以及复杂的迁徙行为。许多鸟类，如候鸟，会形成大规模的迁徙群体 8。迁徙策略具有高度可塑性，栖息地质量会影响个体迁徙的时间和能量预算，进而影响其繁殖和越冬表现，并对种群动态产生影响 9。在觅食过程中，不同物种的鸟类有时会组成混合种群，通过信息共享来提高觅食成功率。理论模型表明，性和社会选择可以稳定动物的合作行为 10。然而，也有一些鸟类，如巢寄生鸟类，会表现出“内向”或非社交的行为，它们将卵产在其他同类巢中，而不提供任何亲代抚育 11。
鱼类：鱼类展现出高度的社交可塑性，其社交行为会根据环境和生理状态进行调整 1213。斑马鱼等鱼类常表现出集体行为，如鱼群（schooling）和群集（shoaling）。鱼群中的个体通过局部互动（如短距离排斥、长距离吸引或对齐）形成高度协调的运动模式 14。这种集群行为被认为是鱼类应对捕食者、提高觅食效率和优化水动力学的适应性策略，体现了其在特定情境下的外向社交倾向。
总的来说，动物的社交倾向并非简单的“有”或“无”，而是在复杂的生态和社会背景下形成的连续谱。从灵长类的高度合作，到大鼠的亲社会行为，再到鸟类和鱼类的集群效应，这些不同的表现形式都体现了物种为了生存和繁衍所采取的适应性策略。高社交倾向的动物往往通过群体合作来获取资源、防御捕食者、提高繁殖成功率，而某些情况下，较少社交或独居的倾向也可能是一种适应性选择。
2. 社交倾向的神经与分子机制
2.1 关键脑区的调控作用
动物的社交倾向受到复杂神经回路的精确调控，其中下丘脑、前额叶皮层（PFC）和腹侧被盖区（VTA）等关键脑区发挥着核心作用。这些脑区通过协调各自的功能，共同调节社交决策、动机和行为的表达。
下丘脑是调控本能社会行为（如性行为、亲代行为和攻击行为）的重要中枢。生殖行为控制柱（Reproductive Behavior Control Column, RBCC）是下丘脑内一个由内侧视前核（MPN）、腹内侧下丘脑腹外侧部（VMHvl）和腹侧乳头状核（PMv）组成的神经回路，对所有社会行为至关重要。RBCC整合了多种激素和代谢信号，并调整动物的身体活动，从而影响社交互动的机会。此外，RBCC还与中脑边缘多巴胺系统相互作用，以维持动物的社交兴趣，并强化与社交行为同步的线索和动作 15。例如，下丘脑室旁核（PVN）中的催产素（OT）神经元被发现是调控群体内社交冲突和攻击行为的关键神经中枢，其活性主要影响雌性动物的攻击性和支配等级，并与奖赏相关的神经回路连接 16。另一项研究表明，针对小细胞催产素（OT）神经元（一种与社交奖赏相关的OT神经元亚型）的胚胎期干扰会导致雄性小鼠的社交功能障碍，提示了这些神经元在社交行为中的选择性脆弱性 17。
前额叶皮层（PFC）在高级社交认知和决策中扮演着关键角色。它与杏仁核等区域的功能交互作用，共同调控社交决策 18。在社交互动过程中，PFC的神经活动会显示出与社交互动相关的脑间同步性，这种同步性可以预测未来的社交互动和竞争情境中的支配关系 19。多巴胺D2受体在内侧前额叶皮层（mPFC）锥体神经元中的表达及其激活会损害小鼠的社交行为，而敲低mPFC锥体神经元中的D2R则能增强社交趋近行为，并选择性地激活投射到伏隔核（NAc）的mPFC神经元 20。这表明PFC通过特定的神经投射，特别是mPFC-NAc通路，精确调控社交行为 20。此外，背内侧前额叶皮层（dmPFC）在调控社交竞争中发挥基础作用，其下游神经回路包括投射到背侧中缝核（DRN）和导水管周围灰质（PAG）的第5层神经元促进竞争，而投射到前基底外侧杏仁核（aBLA）的第2/3层神经元则抑制竞争 21。
腹侧被盖区（VTA）是中脑边缘多巴胺系统的重要组成部分，与社交动机和奖励密切相关。VTA通过多巴胺能投射到伏隔核和前额叶皮层，调节社交奖励的感受和社交行为的强化 22。研究发现，催产素在VTA中的作用对于社交互动的奖赏特性至关重要，VTA中催产素受体的激活能够调节社交互动的强化特性，使其类似食物和滥用药物对行为的强化作用 23。这强调了VTA在将社交互动转化为积极体验方面的关键作用。
神经回路对社交行为的精准调控也容易受到早期环境因素的影响。例如，早期S-氯胺酮暴露会导致青春期小鼠的社交缺陷，这与前额叶皮层（PFC）微胶质细胞的过度激活和突触过度修剪有关 24。S-氯胺酮暴露会激活PFC中的微胶质细胞，导致突触过度修剪和树突结构异常，进而引起兴奋性突触传递的过度兴奋 24。通过下调精氨酸酶1（Arg1）的表达或预防性施用Arg1选择性抑制剂nor-NOHA，可以逆转微胶质细胞的过度激活，并减轻S-氯胺酮暴露引起的神经发育障碍 24。这些发现揭示了特定脑区（如PFC）中的微胶质细胞在发育关键期对社交行为塑造中的关键作用，并为预防麻醉相关的神经发育异常提供了潜在靶点。
2.2 神经递质与激素的介导作用
动物的社交倾向和行为受到多种神经递质和激素的精细调控，这些化学信号在社交奖励、社交动机的形成以及性别差异化的社交偏好中发挥着至关重要的作用。
催产素（Oxytocin, OT）是调控社交行为最为广泛研究的神经肽之一，常被称为“爱情荷尔蒙”或“拥抱荷尔蒙”。它在哺乳动物的依恋、配对结合、性行为、亲代行为以及社交奖励中扮演核心角色 25262728。催产素通过在中枢神经系统中的释放，特别是作用于下丘脑、杏仁核和伏隔核等脑区，来调节社交情绪和行为 26。例如，在以一夫一妻制闻名的草原田鼠中，催产素及其受体的分布模式是其形成伴侣偏好的关键因素之一 2930。脑中催产素的释放能够增强社交奖励，促进个体间的亲社会行为 2531。研究表明，在伏隔核核心区，催产素作为一种社交强化信号，能引起兴奋性突触传递的长期抑制，从而巩固社交互动的奖励特性 31。此外，催产素还通过与多巴胺系统相互作用来调节动机行为，增强社交刺激的动机相关性 25。
多巴胺（Dopamine, DA）是中脑边缘奖励系统的关键神经递质，在社交动机和奖励学习中发挥核心作用 32。伏隔核-中脑回路，作为多巴胺能奖励通路的一部分，与多种形式的社交行为（包括配对结合和亲代行为）的强化密切相关 30。催产素与多巴胺系统之间存在复杂的相互作用，催产素能够影响腹侧被盖区（VTA）的多巴胺能活动，从而进一步调节社交奖励和动机行为 25。例如，VTA中的催产素能调节社交互动的强化特性，使其具有类似食物和药物的奖励效应 25。
血清素（Serotonin, 5-HT）也是重要的神经递质，参与调节情绪、攻击性以及多种社交行为 32。在伏隔核中，血清素与催产素的协调活动对于社交互动的奖励特性至关重要。例如，阻断伏隔核中的5-HT1B受体可以阻止催产素诱导的突触可塑性，进而消除社交奖励效应 31。这表明血清素系统与催产素系统协同作用，共同调节社交奖励的神经机制。
性激素对社交偏好和行为表现出显著的性别差异影响。
- 雌二醇（Estrogen）：雌激素是女性性激素的主要类型，在调节雌性动物的性行为和多种社交行为中起着关键作用 3334。它主要通过与雌激素受体α（ERα）结合来发挥作用，影响多个相互连接的脑区 33。例如，在雌性小鼠中，雌二醇能够调控内侧前额叶皮层（mPFC）中特定神经元的活性，这些神经元整合了激素状态和对潜在配偶的识别，从而协调复杂的认知社交行为 35。发情期的雌性动物，其社交行为受卵巢激素的调节，对异性的社交互动表现出更高的倾向性 3435。
- 睾酮（Testosterone）：作为主要的雄性激素，睾酮及其代谢产物（如雌二醇）在雄性动物的攻击性、领地行为和性行为中扮演重要角色 3637。睾酮水平的变化可以影响社会等级和支配行为，例如在非洲慈鲷中，雄性社会地位的上升与雄激素信号的调节密切相关，雄激素受体拮抗剂会抑制其生殖行为的表达 3637。睾酮的这种影响通常是物种特异性和情境依赖性的 38。
此外，血管加压素（Vasopressin, AVP）是与催产素密切相关的另一种神经肽，在调节社交沟通、社会调查、领地行为和攻击性方面发挥重要作用，尤其是在雄性动物中 2739。血管加压素1a受体（V1aR）在脑区的分布差异与配对结合、配偶保护和空间利用等单配偶制相关行为存在个体和物种差异 29。
这些神经递质和激素通过复杂的交互网络，共同塑造了动物的社交倾向，包括对社交刺激的反应、社交互动中的动机水平以及不同性别在社交行为上的差异 3840。对这些分子机制的深入理解，有助于揭示社交行为障碍的病理生理学基础，并为相关疾病的治疗提供潜在靶点。
2.3 基因与表观遗传的调控基础
动物的社交倾向不仅受神经回路和神经递质的直接影响，更深层地，其根植于复杂的基因表达和表观遗传调控机制。这些机制共同决定了个体对社交刺激的反应模式，并塑造了其终身的社交行为偏好。遗传因素为社交行为提供了基础蓝图，而表观遗传修饰则允许基因表达根据环境变化进行动态调整，从而实现遗传与环境的精妙交互。
基因对社交行为的调控
大量研究表明，特定基因的变异或表达异常与社交行为缺陷，特别是与自闭症谱系障碍（ASD）相关的社交障碍密切相关。ASD是一种神经发育障碍，其核心特征包括社交互动和沟通障碍，以及受限的兴趣、重复行为和活动 41。在动物模型中，一些与ASD相关的基因被发现直接影响社交行为：
- Kcnh7基因：一项研究发现，自闭症模型（Shank3缺陷小鼠）中，Kcnh7基因的表达在小鼠前扣带皮层（ACC）的中间神经元（包括表达小白蛋白PV和生长抑素SST的中间神经元）中显著降低 42。ACC在社交行为中至关重要，其功能障碍与自闭症中的社交互动缺陷有关 42。在PV或SST中间神经元中敲除Kcnh7基因，会导致社交互动缺陷，这表明Kcnh7在调节社交行为中发挥关键作用，且其功能失调可能导致自闭症相关的社交障碍 42。
- CYFIP1同源基因：果蝇中CYFIP1同源基因的突变会导致线粒体过度活跃和群体行为异常。研究发现，线粒体活性增加会捕获GABA，导致GABA能信号传导减少，进而引起社交缺陷。通过药理学或基因手段干预线粒体活性或GABA信号传导，可以纠正这些异常 43。这揭示了与ASD相关的基因可能通过影响细胞代谢和神经递质平衡来调控社交行为。
- 单胺氧化酶A (MAOA) 基因：MAOA基因编码一种降解血清素和儿茶酚胺的关键酶。先天性MAOA缺乏或低活性的MAOA变异体，与攻击性、反社会行为的更高风险相关，尤其是在经历过童年虐待的男性中 44。虽然MAOA主要与攻击性相关，但其通过影响神经递质平衡，也间接影响了社交互动中的情绪调节和行为反应。
表观遗传修饰在社交倾向中的作用
表观遗传学是研究不改变DNA序列但影响基因表达的可遗传变化。环境压力、早期经历和生理状态都可以通过表观遗传机制对社交倾向产生长期影响 45。主要表观遗传修饰包括DNA甲基化、组蛋白修饰和非编码RNA调控 4546。
- 组蛋白乳酰化 (Histone Lactylation)：这是近年来发现的一种新型组蛋白修饰，可以将代谢与基因表达联系起来。一项研究表明，运动诱导的乳酸显著增强了多种突触蛋白的乳酰化，其中突触体相关蛋白91 (SNAP91) 对突触功能至关重要 47。SNAP91的乳酰化通过增强内侧前额叶皮层 (mPFC) 的突触结构形成和神经元活动，从而赋予动物抵抗慢性束缚应激的能力，并预防焦虑样行为 47。尽管这项研究主要关注应激韧性，但mPFC在社交行为中的关键作用表明，组蛋白乳酰化可能间接影响社交倾向，尤其是在应激条件下。
- DNA甲基化：DNA甲基化通过在DNA上添加甲基基团来抑制基因表达，在塑造社交行为中发挥着关键作用 45。例如，母亲行为对后代应激反应能力的影响，被发现与海马区糖皮质激素受体（GR）基因启动子的DNA甲基化模式改变有关。表现出高舔舐和梳理行为的母亲，其后代的GR基因甲基化程度较低，GR表达量较高，从而对压力有更好的适应能力 48。这种表观遗传修饰在成年后仍持续存在，表明早期环境可以“编程”基因表达，进而影响个体对环境的长期适应性，包括社交反应。
- 非编码RNA：微小RNA（miRNAs）是一类小非编码RNA，通过转录后调控影响约60%的基因表达，在神经元功能和社交行为的精细调节中扮演重要角色 49。应激与多种miRNA的表达改变有关，这些改变可能导致应激相关精神疾病，并影响突触功能 49。
遗传与环境的交互作用
社交倾向的形成是遗传 predispositions 和环境因素（如早期经历、社会学习、压力暴露）复杂交互的结果 5051。表观遗传机制正是这种交互作用的桥梁。例如，童年虐待等环境压力被认为是抑郁症发展的重要因素，而表观遗传变化是应激与基因组相互作用导致DNA结构、基因表达和行为稳定改变的关键机制 52。这种基因-环境（G × E）交互作用在孤独症谱系障碍、精神分裂症和焦虑症等多种精神疾病中都有体现，这些疾病常常伴随社交功能障碍 414553。
例如，OXTR基因（催产素受体基因）的多态性与依恋风格和童年虐待之间的基因-环境交互作用有关，并影响社交焦虑症的严重程度 53。OXTR DNA甲基化模式也被认为是连接社交焦虑症各种相关因素的潜在外周生物标志物，突出了表观遗传标记在理解社交障碍中的动态作用 53。
总而言之，动物的社交倾向是由遗传背景提供基础，并受到多种表观遗传机制的动态调控，这些机制使得个体能够根据环境变化调整基因表达，从而灵活适应不断变化的社会环境。深入理解这些复杂的调控网络，对于揭示社交行为的生物学基础，以及开发干预社交功能障碍的方法至关重要。
3. 影响社交倾向的环境与生理因素
3.1 早期经历的长期效应
动物的早期生活经历对其社交倾向的塑造具有深远而持久的影响，这种影响往往通过改变神经发育过程，特别是关键发育期的脑结构和功能，从而对成年期的社交能力产生“环境印记”。早期麻醉暴露、母婴分离和社交隔离是研究早期经历对社交行为长期效应的常用模型。
早期麻醉暴露的影响：
临床研究表明，早期全身麻醉暴露对儿童神经发育的影响最小，但这可能归因于临床前研究的局限性，如缺乏麻醉深度标准、生理监测缺失以及手术损伤未被考虑等 54。然而，在更具临床相关性的动物模型中，研究揭示了早期麻醉暴露对社交行为的潜在长期影响。例如，一项针对小鼠的研究发现，在出生后第17天（PND17）暴露于高浓度七氟烷（一种常见的全身麻醉剂）并伴随手术损伤的小鼠，在成年期（PND56-PND62）表现出微妙但显著的社交能力下降，在三箱实验中，它们对陌生小鼠的偏好显著降低 54。这表明，手术创伤和过深的麻醉深度共同作用，可能导致幼龄小鼠社交行为的长期改变。这些发现强调了发育关键期环境因素，包括医疗干预，对神经发育和社交行为塑造的重要性。
母婴分离的效应：
母婴分离是模拟早期逆境的重要动物模型，已被证实对后代的社交行为产生长期影响。在奶山羊（Capra hircus）的研究中，出生后3天即与母亲分离并人工饲养的幼崽（AR kids），在断奶前表现出更多的玩耍性打斗、奔跑和相互踩踏，但异体梳理行为较少，并且独自休息的时间也少于与母亲共同饲养的幼崽（DR kids）55。断奶后，AR幼崽在与DR幼崽混合后，尽管最初受到DR幼崽更多的攻击，但随着时间的推移，它们似乎逐渐调整了自己的社交行为 55。进一步的长期研究显示，即使在18个月大时，早期母婴分离的奶山羊与未分离的同伴相比，在某些社交互动（如头部轻推）上仍然存在差异，并且在引入陌生群体时，早期分离的个体更容易受到威胁 56。
在大鼠模型中，长时间的母婴分离（例如出生后1-21天每天分离360分钟，MS360）对青春期雄性大鼠的社交玩耍行为和皮质酮水平产生了显著影响，但对雌性大鼠则无明显影响 57。MS360的雄性大鼠表现出更高的基础和恢复期皮质酮水平，以及更多的社交玩耍行为，例如“压制”（pinning）动作 57。这些性别特异性效应揭示了早期逆境对不同性别个体社交行为和应激反应轴的差异化影响。
社交隔离的影响：
社交隔离，特别是在青少年关键发育期，被证明对大脑功能和行为产生深远影响。青少年期是社交技能发展的敏感时期，期间的社交隔离会对成年期的社交技能发展和心理健康造成破坏性影响 5859。例如，对雄性小鼠而言，青少年期一周的社交隔离会增加社交互动，但却损害了社交习惯化和社交新颖性偏好，这表现为对新奇刺激的反应不足 58。行为上的改变伴随着腹侧被盖区（VTA）多巴胺（pDA）神经元的急性过度兴奋，以及投射到前额叶皮层（PFC）的pDA神经元突触中缺乏GluA2的AMPARs的长期表达 58。令人注意的是，通过化学遗传学方法抑制下丘脑室旁核（PVN）中的催产素神经元，可以逆转社交隔离引起的行为缺陷以及神经活动和突触可塑性的改变 58。这表明催产素神经元介导了社交隔离对VTA回路的影响，进一步凸显了早期社交环境对关键神经回路重塑的重要性。
微胶质细胞与突触修剪的机制：
上述早期经历的长期效应，特别是社交缺陷，往往与发育关键期内神经元的异常重塑有关。微胶质细胞作为中枢神经系统的免疫细胞，在发育过程中参与突触修剪，即移除多余或功能不佳的突触，以优化神经回路的连接 60。环境因素如产前暴露于丙戊酸（VPA）——一种自闭症模型常用的诱导剂——通过降低外泌体miRNA（特别是miR-215-5p）的表达，激活NEAT1/MAPK1/p-CRMP2通路，导致过度的突触修剪和异常的突触成熟，最终导致社交功能障碍 60。这些研究共同阐明了发育关键期环境因素（如药物、压力、隔离）如何通过改变微胶质细胞介导的突触修剪过程，对神经回路的发育和成熟产生负面影响，从而在动物的社交能力上留下“环境印记”。
3.2 环境压力与资源分布
环境压力和资源分布是塑造动物社交模式的关键生态因素，它们通过影响个体生存和繁殖的成本效益，驱动动物形成不同的集体行为。这些外部条件可以显著改变动物的社交倾向，促使它们采取更聚集或更分散的生活方式，以适应不断变化的环境挑战。
水体环境与鱼类集体行为：
在水生环境中，斑马鱼（Danio rerio）作为一种高度社会化的鱼类，其集体行为如鱼群（schooling）和群集（shoaling）会受到环境因素的影响。斑马鱼在14日龄后即可展现出多种非繁殖性社会行为，包括位置偏好、定向以及社会提示等 61。环境中的污染物也会改变斑马鱼的社交行为。例如，杀虫剂fenpropathrin暴露会导致斑马鱼焦虑水平升高，并促使它们更多地聚集在同类区域，这可能是一种寻求安慰或减少感知风险的行为 62。这表明，水体环境的改变，无论是物理性的水流，还是化学性的污染物，都能直接影响鱼类的社交偏好和集体行为。
食物资源分布与灵长类社交模式：
食物资源的可用性和分布模式对灵长类动物的社交结构和社交容忍度有深远影响。在野外环境中，觅食者面临着社会（如等级排名）和生态（如食物可得性和分布）双重挑战，这些因素共同影响它们的觅食决策和成功率。例如，普通狨猴（Callithrix jacchus）是一种合作繁殖的灵长类动物，它们在觅食点的社交容忍度会因食物分布（集中或分散）和产量（高、中、低）的不同而变化 63。研究发现，当食物集中在单一地点时，狨猴的觅食关联网络更加紧密，个体间协作觅食的频率和强度增加。尽管个体在获得食物后会选择远离群体消费，但共同占据觅食点能让它们获得更多食物。这表明，在食物资源集中且竞争预期最高的情况下，狨猴反而表现出更高的社交容忍度，以维持群体的凝聚力，提高获取资源的效率 63。这种行为策略有助于它们在资源受限的环境中实现互利共赢，并增强后代的生存机会。
群体密度对社交行为的影响：
群体密度是影响动物社交行为的另一个重要环境因素。
- 种群密度与栖息地特化：种群密度对动物的栖息地选择和社会行为都会产生密度依赖性效应。在加拿大驯鹿（Rangifer tarandus）的研究中发现，在高密度种群中，栖息地特化者（即高度依赖特定栖息地的个体）比广食性个体具有更高的年度繁殖成功率，但它们也比广食性个体更不爱社交 64。这可能表明，特化者通过减少社交来避免高密度下的资源竞争。这项研究支持了生态位变异假说，即密度依赖性栖息地特化是一种适应性机制 64。
- 饲养密度与动物福利：在圈养环境中，饲养密度对动物的社交互动和福利有着直接影响。例如，在奶牛（Bos taurus）的研究中，饲养密度与采食行为和社会行为密切相关。当采食槽的牛只密度增加时，奶牛的采食时间减少，无活动站立时间增加，并且被同伴驱赶的频率更高 65。社会等级较低的牛只在拥挤的采食环境中更容易被驱赶。这表明高密度会增加牛只间的竞争和攻击性，降低采食效率。此外，即使是被认为是独居的动物，如红腿陆龟（Chelonoidis carbonaria），其社交行为也受饲养密度影响。研究发现，当饲养密度从两只增加到四只时，陆龟的攻击性行为（主要是骑跨）显著增加，并且利用围栏的范围也更广 66。这提示我们，即使是独居物种，高密度环境也可能诱发或加剧社交冲突，对其福利产生负面影响。
- 城市化对社交行为的重塑：城市化是全球性的环境变化，它将动物暴露在新的生态条件下，从而改变其社交互动的频率和性质。城市栖息地的特征，如人造基础设施和斑块状的资源分布，可能会限制动物的移动，促进聚集，从而增加同类个体之间的接触 67。例如，对普通壁虎（Podarcis muralis）的研究发现，城市中的壁虎比非城市环境中的壁虎拥有更多的社会联系，更强的关联，并且总体上参与更多的社会互动 67。这些差异并非由种群密度变化解释。研究者提出，城市栖息地的空间限制和资源异质性可能增强了壁虎的社交容忍度。这表明，城市化甚至可以重塑非群居物种的社交行为，而社交策略的转变可能是它们在城市景观中生存下来的重要因素 67。
综上所述，环境压力和资源分布通过调节生存和繁殖的成本效益，直接影响动物的社交倾向和集体行为。从水生生物的鱼群行为到陆生动物的觅食策略和栖息地选择，再到圈养环境和城市化对社交互动的影响，都体现了动物在面对不同环境挑战时，社交模式所展现出的高度适应性和可塑性。
3.3 生理状态与代谢调控
动物的生理状态和内部代谢过程对社交倾向有着深远的影响，特别是通过肠脑轴（gut-brain axis）的调节以及能量代谢的动态变化。这些生理机制不仅影响个体的社交动机和行为表达，还可能在神经发育障碍相关的社交缺陷中发挥关键作用。
肠道菌群与社交行为的调节
肠道菌群作为宿主生理和行为的调节者，通过复杂的肠脑轴与社交行为密切相关。研究表明，肠道菌群的失调与多种神经发育和精神疾病（如自闭症谱系障碍，ASD）中的社交缺陷有关。
- ASD模型中的肠道菌群与社交功能：在ASD动物模型中，肠道菌群的组成和功能异常被广泛观察到。例如，母源高脂饮食（MHFD）诱导的后代，其肠道菌群失调，并表现出社交缺陷。通过与正常饮食母亲的后代合笼饲养，或进行粪便微生物群移植（FMT），可以纠正MHFD后代的肠道菌群失调和社交缺陷 68。这表明肠道菌群在介导母体饮食对后代神经发育影响中具有因果关系。
- 益生菌的干预作用：特定的益生菌株对社交行为具有积极影响。例如，鼠李糖乳杆菌（Lactobacillus reuteri）被发现能够选择性地改善多种遗传、环境和特发性ASD模型小鼠的社交缺陷 69。有趣的是，这种作用并非通过恢复宿主肠道菌群组成来实现，而是通过迷走神经依赖的方式，恢复ASD小鼠腹侧被盖区（VTA）社交互动诱导的突触可塑性 69。此外，有研究表明，肠道微生物群中的某些特定细菌，如粪链球菌（Streptococcus vestibularis），可以导致小鼠的社交行为缺陷，并改变外周组织中的神经递质水平，这提示了微生物-脑轴在精神分裂症等疾病中扮演的角色 70。
- 短链脂肪酸（SCFAs）与高纤维饮食：肠道菌群发酵膳食纤维产生的短链脂肪酸（如丁酸、丙酸、乙酸）是重要的代谢产物，能够通过肠脑轴影响宿主生理。一项针对母体肥胖的研究发现，母体肥胖会导致后代的行为和肠道菌群异常，而高纤维饮食（无论是母体还是后代摄入）可以通过改善突触损伤和微胶质细胞成熟缺陷来恢复这些异常 71。短链脂肪酸的治疗也能够缓解肥胖母亲后代的行为缺陷 71。此外，高纤维饮食还可以降低青少年胰岛素抵抗的几率 72，而胰岛素抵抗与某些神经认知功能受损有关，间接影响社交功能。在猪的妊娠期，饲喂高纤维饮食的母猪所产下的仔猪，在断奶前具有更少的皮肤损伤，这表明其攻击性行为减少，可能与肠道菌群通过肠脑轴对行为的调节有关 73。
能量代谢与社交动机
能量代谢状态也与社交动机和行为密切相关。动物的能量水平和代谢产物可以作为内在信号，影响大脑对社交奖励的处理和社交行为的投入。
- 乳酸水平与社交动机：乳酸作为一种重要的能量代谢产物，不仅在肌肉运动中发挥作用，也被发现与神经活动和社交动机存在关联。研究表明，在激烈运动后，血液乳酸水平会升高 74。虽然现有研究多聚焦于乳酸与运动恢复和认知功能的关系 75，但乳酸作为一种可跨越血脑屏障的代谢物，其在大脑中的浓度变化可能会影响神经递质的合成和释放，进而调控社交动机。例如，在应激状态下，动物的能量代谢会发生改变，这可能影响其社交行为。饥饿等生理应激会影响动物的攻击性行为和激素水平 76。在禁食24小时的猪中，相比于饱食的猪，表现出更多的服从行为，尽管在打斗中皮质醇和儿茶酚胺水平的升高相似，但饥饿抑制了应激诱导的高血糖反应 76。这提示了能量状态对社交等级和互动模式的影响。
- 黏膜真菌与社交行为：肠道黏膜相关真菌（MAF）不仅能增强肠道屏障功能，还能通过与17型免疫反应的相互作用促进小鼠的社交行为 77。真菌对肠道局部屏障功能的影响依赖于CD4 T辅助细胞产生的IL-22，而其对社交行为的影响则通过神经元中IL-17R依赖性信号介导 77。这揭示了肠道微生物群，包括真菌，可以通过免疫系统和神经通路，在社交行为的调节中发挥直接作用。
综上所述，生理状态和代谢调控通过多条途径影响动物的社交倾向。肠道菌群及其代谢产物（如短链脂肪酸）通过肠脑轴对社交行为进行精细调节，而能量代谢产物（如乳酸）也可能作为信号分子影响社交动机。这些内在生理机制的深入研究，不仅有助于我们理解动物社交行为的生物学基础，也为干预社交障碍提供了新的靶点和策略。
4. 高社交倾向动物的共性特征与进化意义
4.1 高社交动物的行为与生态共性
高社交倾向的动物，无论是通过复杂的社会结构还是简单的聚集行为，都展现出一些共性的行为模式和生态适应策略。这些特征使得它们能够更好地应对环境挑战，提高生存和繁殖的成功率。
合作繁殖是高社交倾向动物的典型特征之一，尤其在某些物种中表现突出。例如，草原田鼠（prairie voles）以其严格的一夫一妻制和高度的亲代投资而闻名，雄性田鼠不仅参与筑巢、孵育，还积极守护幼崽，共同抚养后代。这种合作繁殖模式显著提高了后代的存活率，是其社会化生活方式的核心体现。在灵长类动物中，如狨猴（marmosets）和柽柳猴（tamarins），也存在合作繁殖的现象，群体成员（包括非繁殖个体）会帮助抚养幼崽，分担育儿成本 78。这种模式通过增加可用的照料者数量，有效减轻了育儿负担，并促进了群体的稳定和扩展。
群体防御是高社交动物普遍采用的生存策略。通过集群，个体能够更有效地发现并抵御捕食者。例如，灵长类动物在群体觅食或休息时，常有“哨兵”行为，即有成员站岗放哨，一旦发现危险便发出警报，使得整个群体能够迅速做出反应，或逃跑，或集体驱赶捕食者。斑鬣狗（spotted hyenas）也展现出高度的社会性，它们通过群体合作狩猎大型猎物，并能有效防御其他捕食者的竞争 79。群体防御不仅提高了单个个体的存活率，也增强了整个种群的适应性。
信息共享是高社交动物在觅食、避险和学习过程中不可或缺的行为。在鸟类中，不同物种有时会形成混合种群进行觅食，通过相互观察和信号交流，共享关于食物来源和潜在威胁的信息。这种信息共享能够提高觅食效率，减少捕食风险。例如，当一个鸟类个体发现丰富的食物源时，可能会通过特定的叫声吸引其他同伴，从而使整个群体受益。在蚁群或蜜蜂等社会性昆虫中，信息素和舞蹈等复杂的交流方式，使得群体能够高效地共享资源位置信息，协调集体行动。此外，复杂的社会行为还依赖于认知技能，如个体识别和观察学习，这些技能是社会系统进化的基础。
总而言之，高社交倾向的动物通过合作繁殖、群体防御和信息共享等行为模式，形成了紧密的社会联系。这些行为不仅增加了每个个体的生存机会，还优化了资源的获取和利用，增强了群体应对环境变化的能力。它们共同的生存策略体现了“集体大于个体”的原则，是其在长期进化过程中形成的有效适应性选择。这些共性特征反映了社交性在多种动物类群中作为一种成功的进化策略的普遍价值。
4.2 社交倾向的进化选择压力
社交倾向的进化适应性意义在于，它通过增强群体凝聚力、优化资源获取和促进基因传递等机制，为个体和种群带来了显著的生存和繁殖优势，从而在自然选择中被保留和强化。
增强群体凝聚力与种群存活率
高度的社交倾向使得动物能够形成更紧密的群体，这种群体凝聚力在面临外部威胁时尤为关键。群体合作可以显著提升个体抵御捕食者的能力，例如，外群冲突对社会物种来说是一种强大的选择压力，它可能带来生存和繁殖上的后果 80。
此外，群体的存在本身就能提供社会支持，减轻个体压力。催产素作为一种应激应对分子，其内源性作用和对催产素受体的刺激支持生长、恢复力和愈合，并且在逆境或创伤面前具有保护作用，这可能解释了积极社会经验的益处 81。在哺乳动物中，自主神经系统的神经调节发生了系统发育上的转变，这产生了一个神经解剖学上整合的社会参与系统，包括调节心迷走神经张力以及参与发声的肌肉的神经机制 82。自主神经状态与婴儿哭声声学特征的共变关系研究表明，生理状态与发声的声学频率之间存在神经生理学基础的联系，这表明社会行为和生理反应之间存在密切联系 83。虽然动物研究中的直接证据较少，但群居生活带来的社会互动和支持无疑有助于个体在面对环境挑战时保持更好的生理和心理状态，从而间接提升存活率。
优化资源获取
社交行为还能显著提高动物获取和利用资源（如食物、水、庇护所）的效率。
鱼类集群觅食效率：许多鱼类物种会形成鱼群进行觅食。集群行为不仅能有效规避捕食者，还能通过集体搜寻和信息共享，提高觅食的整体效率。当一个鱼群中的某个个体发现食物来源时，其他个体可以迅速响应，共同利用资源。混合物种群体（MSGs）被广泛认为能提高捕食者规避和觅食效率，从而增加参与者的适应度 84。此外，雌性阿德利企鹅的日捕获率和单位努力捕获量在所有年龄段都低于雄性，但雌性在觅食表现方面显示出持续的个体改善 85。
合作狩猎：在一些捕食性物种中，如狼和非洲野狗，群体合作狩猎能够捕捉到单个个体无法制服的大型猎物。这种合作不仅增加了捕食成功率，也确保了群体成员的食物供应，优化了能量获取。
信息共享：在一些混合物种群中，不同物种的动物会共享关于食物和威胁的信息 84。例如，鸟类在混合种群中觅食时，能够通过观察和倾听同伴的信号，更有效地发现食物并规避风险。这种信息共享极大地提升了群体的整体资源利用效率。
促进基因传递与性选择
社交倾向也在基因传递，特别是通过性选择中发挥着关键作用。
性选择中的社交展示：许多物种中，雄性通过复杂的求偶展示来吸引雌性，这些展示往往具有高度的社交性。例如，孔雀雄性通过炫耀其华丽的尾屏来吸引雌性。在评估竞争对手时，雄性孔雀会选择性地关注其竞争者的展示区域，这表明孔雀在评估竞争对手时会选择性地分配注意力 86。虽然求偶展示往往被认为是选择最强壮的雄性，但有时微妙的展示，即“羞涩”行为，也可能在性选择中发挥作用 87。雌性往往倾向于选择那些拥有最“活力四射”或最能反映其品质的雄性，这促使雄性不断进化出更具吸引力的社交展示行为 88。
社会地位与繁殖成功：在许多社会等级制度严明的物种中，高社会地位的个体往往拥有更高的繁殖成功率。非侵入性技术可以帮助研究人员在自然环境中监测动物的荷尔蒙行为互动，这对于研究社会策略的成本、竞争的成本和侵略性，以及气质在个体繁殖成功中的作用等方面具有重要意义 89。例如，水黾（Microvelia longipes）的雄性通过竞争产卵点，并利用其长长的后腿作为武器来压制竞争者，从而获得与雌性交配的机会。研究发现，当产卵点资源有限时，小型雄性只能使大约5%的卵受精，而当产卵点充足时，这一比例会增加到约20% 90。这表明社交竞争中的优势可以直接转化为基因传递的成功。
合作与繁衍：在人类等高度合作的物种中，合作行为本身成为一种重要的进化选择压力。人类合作的原则与多细胞生物的演化相似，包括分工、沟通和适应度相互依赖 91。这种强烈的合作倾向使得早期人类能够形成复杂的社会结构，发展出文化和技术，最终导致了爆炸性的人口增长和巨大的群体合作能力 91。通过合作，个体能够获取更大的利益，例如共同抚养后代，分享资源，从而间接提升了每个个体基因传递的成功率。
综上所述，社交倾向的进化意义在于它为动物提供了强大的适应性优势，使其能够更好地在多变的自然环境中生存和繁衍。无论是通过群体合作抵御威胁，集体觅食提高效率，还是通过性选择中的社交展示促进基因传递，社交行为都是物种成功的关键驱动力。自然选择持续筛选那些能够有效参与社交互动的个体，从而塑造了动物界中多样而复杂的社交行为模式。
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Trends Ecol Evol. 2019 Feb;34(2):112-120. doi: 10.1016/j.tree.2018.11.006. Epub 2018 Dec 7.
Theoretical models show that sexual and social selection can stabilise cooperation. However, field tests of these mechanisms have been difficult to conduct and the results are mixed. We discuss the conceptual and practical difficulties associated with testing the role of social and sexual selection on cooperation and argue that there are alternative ways of examining these hypotheses. Specifically, approaches based on the classic theories of sexual selection and signalling, and recent developments in the field of behavioural syndromes, provide mechanisms to insure the reliability of cooperation. In addition, methodological developments (social networks and microtracking) and long-term datasets, allow measuring partner choice in a cooperation context and the resulting fitness benefits for both the cooperators and the individuals that associate with them.
11Conspecific brood parasitism and population dynamics.PubMed
Perry de Valpine, John M Eadie
Am Nat. 2008 Oct;172(4):547-62. doi: 10.1086/590956.
Conspecific brood parasitism (CBP), defined as parasitic laying of eggs in a conspecific nest without providing parental care, occurs in insects, fishes, amphibians, and many birds. Numerous factors have been proposed to influence the evolution of CBP, including nest site limitation; effects of brood size, laying order, or parasitic status on offspring survival; randomness of parasitic egg distribution; adult life-history trade-offs; and variation in parental female quality or risk of nest predation. However, few theoretical studies consider multiple possible types of parasitism or the interplay between evolution of parasitism and population dynamics. We review existing theory of CBP and develop a synthetic modeling approach to ask how best-of-a-bad job parasitism, separate-strategies parasitism (in which females either nest or parasitize), and joint-strategies parasitism (in which females can both nest and parasitize) differ in their evolutionary conditions and impacts on population dynamics using an adaptive dynamics framework including multivariate traits. CBP can either stabilize or destabilize population dynamics in different scenarios, and the role of comparable parameters on evolutionarily stable strategy parasitism rate, equilibrium population size, and population stability can differ for the different modes of parasitism.
12Social plasticity in fish: integrating mechanisms and function.PubMed
R F Oliveira
J Fish Biol. 2012 Dec;81(7):2127-50. doi: 10.1111/j.1095-8649.2012.03477.x. Epub 2012 Nov 27.
Social plasticity is a ubiquitous feature of animal behaviour. Animals must adjust the expression of their social behaviour to the nuances of daily social life and to the transitions between life-history stages, and the ability to do so affects their Darwinian fitness. Here, an integrative framework is proposed for understanding the proximate mechanisms and ultimate consequences of social plasticity. According to this framework, social plasticity is achieved by rewiring or by biochemically switching nodes of the neural network underlying social behaviour in response to perceived social information. Therefore, at the molecular level, it depends on the social regulation of gene expression, so that different brain genomic and epigenetic states correspond to different behavioural responses and the switches between states are orchestrated by signalling pathways that interface the social environment and the genotype. At the evolutionary scale, social plasticity can be seen as an adaptive trait that can be under positive selection when changes in the environment outpace the rate of genetic evolutionary change. In cases when social plasticity is too costly or incomplete, behavioural consistency can emerge by directional selection that recruits gene modules corresponding to favoured behavioural states in that environment. As a result of this integrative approach, how knowledge of the proximate mechanisms underlying social plasticity is crucial to understanding its costs, limits and evolutionary consequences is shown, thereby highlighting the fact that proximate mechanisms contribute to the dynamics of selection. The role of teleosts as a premier model to study social plasticity is also highlighted, given the diversity and plasticity that this group exhibits in terms of social behaviour. Finally, the proposed integrative framework to social plasticity also illustrates how reciprocal causation analysis of biological phenomena (i.e. considering the interaction between proximate factors and evolutionary explanations) can be a more useful approach than the traditional proximate-ultimate dichotomy, according to which evolutionary processes can be understood without knowledge on proximate causes, thereby black-boxing developmental and physiological mechanisms.
13Social plasticity in the fish brain: Neuroscientific and ethological aspects.PubMed
Karen Maruska, Marta C Soares, Monica Lima-Maximino, et al.
Brain Res. 2019 May 15;1711:156-172. doi: 10.1016/j.brainres.2019.01.026. Epub 2019 Jan 23.
Social plasticity, defined as the ability to adaptively change the expression of social behavior according to previous experience and to social context, is a key ecological performance trait that should be viewed as crucial for Darwinian fitness. The neural mechanisms for social plasticity are poorly understood, in part due to skewed reliance on rodent models. Fish model organisms are relevant in the field of social plasticity for at least two reasons: first, the diversity of social organization among fish species is staggering, increasing the breadth of evolutionary relevant questions that can be asked. Second, that diversity also suggests translational relevance, since it is more likely that "core" mechanisms of social plasticity are discovered by analyzing a wider variety of social arrangements than relying on a single species. We analyze examples of social plasticity across fish species with different social organizations, concluding that a "core" mechanism is the initiation of behavioral shifts through the modulation of a conserved "social decision-making network", along with other relevant brain regions, by monoamines, neuropeptides, and steroid hormones. The consolidation of these shifts may be mediated via neurogenomic adjustments and regulation of the expression of plasticity-related molecules (transcription factors, cell cycle regulators, and plasticity products).
14Collective behavior from surprise minimization.PubMed
Conor Heins, Beren Millidge, Lancelot Da Costa, et al.
Proc Natl Acad Sci U S A. 2024 Apr 23;121(17):e2320239121. doi: 10.1073/pnas.2320239121. Epub 2024 Apr 17.
Collective motion is ubiquitous in nature; groups of animals, such as fish, birds, and ungulates appear to move as a whole, exhibiting a rich behavioral repertoire that ranges from directed movement to milling to disordered swarming. Typically, such macroscopic patterns arise from decentralized, local interactions among constituent components (e.g., individual fish in a school). Preeminent models of this process describe individuals as self-propelled particles, subject to self-generated motion and "social forces" such as short-range repulsion and long-range attraction or alignment. However, organisms are not particles; they are probabilistic decision-makers. Here, we introduce an approach to modeling collective behavior based on active inference. This cognitive framework casts behavior as the consequence of a single imperative: to minimize surprise. We demonstrate that many empirically observed collective phenomena, including cohesion, milling, and directed motion, emerge naturally when considering behavior as driven by active Bayesian inference-without explicitly building behavioral rules or goals into individual agents. Furthermore, we show that active inference can recover and generalize the classical notion of social forces as agents attempt to suppress prediction errors that conflict with their expectations. By exploring the parameter space of the belief-based model, we reveal nontrivial relationships between the individual beliefs and group properties like polarization and the tendency to visit different collective states. We also explore how individual beliefs about uncertainty determine collective decision-making accuracy. Finally, we show how agents can update their generative model over time, resulting in groups that are collectively more sensitive to external fluctuations and encode information more robustly.
15Hypothalamic control of innate social behaviors.PubMed
Long Mei, Takuya Osakada, Dayu Lin
Science. 2023 Oct 27;382(6669):399-404. doi: 10.1126/science.adh8489. Epub 2023 Oct 26.
Sexual, parental, and aggressive behaviors are central to the reproductive success of individuals and species survival and thus are supported by hardwired neural circuits. The reproductive behavior control column (RBCC), which comprises the medial preoptic nucleus (MPN), the ventrolateral part of the ventromedial hypothalamus (VMHvl), and the ventral premammillary nucleus (PMv), is essential for all social behaviors. The RBCC integrates diverse hormonal and metabolic cues and adjusts an animal's physical activity, hence the chance of social encounters. The RBCC further engages the mesolimbic dopamine system to maintain social interest and reinforces cues and actions that are time-locked with social behaviors. We propose that the RBCC and brainstem form a dual-control system for generating moment-to-moment social actions. This Review summarizes recent progress regarding the identities of RBCC cells and their pathways that drive different aspects of social behaviors.
16Sexually dimorphic oxytocin circuits drive intragroup social conflict and aggression in wild house mice.PubMed
Yizhak Sofer, Noga Zilkha, Elena Gimpel, et al.
Nat Neurosci. 2024 Aug;27(8):1565-1573. doi: 10.1038/s41593-024-01685-5. Epub 2024 Jul 5.
In nature, both males and females engage in competitive aggressive interactions to resolve social conflicts, yet the behavioral principles guiding such interactions and their underlying neural mechanisms remain poorly understood. Through circuit manipulations in wild mice, we unveil oxytocin-expressing (OT) neurons in the hypothalamic paraventricular nucleus (PVN) as a neural hub governing behavior in dyadic and intragroup social conflicts, influencing the degree of behavioral sexual dimorphism. We demonstrate that OT PVN neurons are essential and sufficient in promoting aggression and dominance hierarchies, predominantly in females. Furthermore, pharmacogenetic activation of these neurons induces a change in the 'personality' traits of the mice within groups, in a sex-dependent manner. Finally, we identify an innervation from these OT neurons to the ventral tegmental area that drives dyadic aggression, in a sex-specific manner. Our data suggest that competitive aggression in naturalistic settings is mediated by a sexually dimorphic OT network connected with reward-related circuitry.
17Selective vulnerability of parvocellular oxytocin neurons in social dysfunction.PubMed
Masafumi Tsurutani, Teppei Goto, Mitsue Hagihara, et al.
Nat Commun. 2024 Oct 6;15(1):8661. doi: 10.1038/s41467-024-53092-w.
Selective vulnerability offers a conceptual framework for understanding neurodegenerative disorders such as Parkinson's disease, where specific neuronal types are selectively affected and adjacent ones are spared. However, the applicability of this framework to neurodevelopmental disorders, particularly those characterized by atypical social behaviors, such as autism spectrum disorder, remains uncertain. Here we show that an embryonic disturbance, known to induce social dysfunction in male mice, preferentially impaired the gene expression crucial for neural functions in parvocellular oxytocin (OT) neurons-a subtype linked to social rewards-while neighboring cell types experienced a lesser impact. Chemogenetic stimulation of OT neurons at the neonatal stage ameliorated social deficits in early adulthood, concurrent with cell-type-specific sustained recovery of pivotal gene expression within parvocellular OT neurons. Collectively, our data shed light on the transcriptomic selective vulnerability within the hypothalamic social behavioral center and provide a potential therapeutic target through specific neonatal neurostimulation.
18Prefrontal-amygdala circuits in social decision-making.PubMed
Prabaha Gangopadhyay, Megha Chawla, Olga Dal Monte, et al.
Nat Neurosci. 2021 Jan;24(1):5-18. doi: 10.1038/s41593-020-00738-9. Epub 2020 Nov 9.
An increasing amount of research effort is being directed toward investigating the neural bases of social cognition from a systems neuroscience perspective. Evidence from multiple animal species is beginning to provide a mechanistic understanding of the substrates of social behaviors at multiple levels of neurobiology, ranging from those underlying high-level social constructs in humans and their more rudimentary underpinnings in monkeys to circuit-level and cell-type-specific instantiations of social behaviors in rodents. Here we review literature examining the neural mechanisms of social decision-making in humans, non-human primates and rodents, focusing on the amygdala and the medial and orbital prefrontal cortical regions and their functional interactions. We also discuss how the neuropeptide oxytocin impacts these circuits and their downstream effects on social behaviors. Overall, we conclude that regulated interactions of neuronal activity in the prefrontal-amygdala pathways critically contribute to social decision-making in the brains of primates and rodents.
19Correlated Neural Activity and Encoding of Behavior across Brains of Socially Interacting Animals.PubMed
Lyle Kingsbury, Shan Huang, Jun Wang, et al.
Cell. 2019 Jul 11;178(2):429-446.e16. doi: 10.1016/j.cell.2019.05.022. Epub 2019 Jun 20.
Social interactions involve complex decision-making tasks that are shaped by dynamic, mutual feedback between participants. An open question is whether and how emergent properties may arise across brains of socially interacting individuals to influence social decisions. By simultaneously performing microendoscopic calcium imaging in pairs of socially interacting mice, we find that animals exhibit interbrain correlations of neural activity in the prefrontal cortex that are dependent on ongoing social interaction. Activity synchrony arises from two neuronal populations that separately encode one's own behaviors and those of the social partner. Strikingly, interbrain correlations predict future social interactions as well as dominance relationships in a competitive context. Together, our study provides conclusive evidence for interbrain synchrony in rodents, uncovers how synchronization arises from activity at the single-cell level, and presents a role for interbrain neural activity coupling as a property of multi-animal systems in coordinating and sustaining social interactions between individuals.
20Dopamine D2 receptors in pyramidal neurons in the medial prefrontal cortex regulate social behavior.PubMed
Hao Chen, Xing-Xing Xiong, Shi-Yang Jin, et al.
Pharmacol Res. 2024 Jan;199:107042. doi: 10.1016/j.phrs.2023.107042. Epub 2023 Dec 22.
Drugs acting on dopamine D2 receptors are widely used for the treatment of several neuropsychiatric disorders, including schizophrenia and depression. Social deficits are a core symptom of these disorders. Pharmacological manipulation of dopamine D2 receptors (Drd2), a Gi-coupled subtype of dopamine receptors, in the medial prefrontal cortex (mPFC) has shown that Drd2 is implicated in social behaviors. However, the type of neurons expressing Drd2 in the mPFC and the underlying circuit mechanism regulating social behaviors remain largely unknown. Here, we show that Drd2 were mainly expressed in pyramidal neurons in the mPFC and that the activation of the Gi-pathway in Drd2 pyramidal neurons impaired social behavior in male mice. In contrast, the knockdown of D2R in pyramidal neurons in the mPFC enhanced social approach behaviors in male mice and selectively facilitated the activation of mPFC neurons projecting to the nucleus accumbens (NAc) during social interaction. Remarkably, optogenetic activation of mPFC-to-NAc-projecting neurons mimicked the effects of conditional D2R knockdown on social behaviors. Altogether, these results demonstrate a cell type-specific role for Drd2 in the mPFC in regulating social behavior, which may be mediated by the mPFC-to-NAc pathway.
21Deconstructing the neural circuit underlying social hierarchy in mice.PubMed
Qiuhong Xin, Diyang Zheng, Tingting Zhou, et al.
Neuron. 2025 Feb 5;113(3):444-459.e7. doi: 10.1016/j.neuron.2024.11.007. Epub 2024 Dec 10.
Social competition determines hierarchical social status, which profoundly influences animals' behavior and health. The dorsomedial prefrontal cortex (dmPFC) plays a fundamental role in regulating social competitions, but it was unclear how the dmPFC orchestrates win- and lose-related behaviors through its downstream neural circuits. Here, through whole-brain c-Fos mapping, fiber photometry, and optogenetics- or chemogenetics-based manipulations, we identified anatomically segregated win- and lose-related neural pathways downstream of the dmPFC in mice. Specifically, layer 5 neurons projecting to the dorsal raphe nucleus (DRN) and periaqueductal gray (PAG) promote social competition, whereas layer 2/3 neurons projecting to the anterior basolateral amygdala (aBLA) suppress competition. These two neuronal populations show opposite changes in activity during effortful pushes in competition. In vivo and in vitro electrophysiology recordings revealed inhibition from the lose-related pathway to the win-related pathway. Such antagonistic interplay may represent a central principle in how the mPFC orchestrates complex behaviors through top-down control.
22Social circuits and their dysfunction in autism spectrum disorder.PubMed
Masaaki Sato, Nobuhiro Nakai, Shuhei Fujima, et al.
Mol Psychiatry. 2023 Aug;28(8):3194-3206. doi: 10.1038/s41380-023-02201-0. Epub 2023 Aug 24.
Social behaviors, how individuals act cooperatively and competitively with conspecifics, are widely seen across species. Rodents display various social behaviors, and many different behavioral paradigms have been used for investigating their neural circuit bases. Social behavior is highly vulnerable to brain network dysfunction caused by neurological and neuropsychiatric conditions such as autism spectrum disorders (ASDs). Studying mouse models of ASD provides a promising avenue toward elucidating mechanisms of abnormal social behavior and potential therapeutic targets for treatment. In this review, we outline recent progress and key findings on neural circuit mechanisms underlying social behavior, with particular emphasis on rodent studies that monitor and manipulate the activity of specific circuits using modern systems neuroscience approaches. Social behavior is mediated by a distributed brain-wide network among major cortical (e.g., medial prefrontal cortex (mPFC), anterior cingulate cortex, and insular cortex (IC)) and subcortical (e.g., nucleus accumbens, basolateral amygdala (BLA), and ventral tegmental area) structures, influenced by multiple neuromodulatory systems (e.g., oxytocin, dopamine, and serotonin). We particularly draw special attention to IC as a unique cortical area that mediates multisensory integration, encoding of ongoing social interaction, social decision-making, emotion, and empathy. Additionally, a synthesis of studies investigating ASD mouse models demonstrates that dysfunctions in mPFC-BLA circuitry and neuromodulation are prominent. Pharmacological rescues by local or systemic (e.g., oral) administration of various drugs have provided valuable clues for developing new therapeutic agents for ASD. Future efforts and technological advances will push forward the next frontiers in this field, such as the elucidation of brain-wide network activity and inter-brain neural dynamics during real and virtual social interactions, and the establishment of circuit-based therapy for disorders affecting social functions.
23Role of oxytocin in the ventral tegmental area in social reinforcement.PubMed
Johnathan M Borland, Kymberly N Grantham, Lauren M Aiani, et al.
Psychoneuroendocrinology. 2018 Sep;95:128-137. doi: 10.1016/j.psyneuen.2018.05.028. Epub 2018 May 21.
The rewarding properties of social interactions play a critical role in the development and maintenance of social relationships, and deficits in social reward are associated with various psychiatric disorders. In the present study, we used a novel Operant Social Preference (OSP) task to investigate the reinforcing properties of social interactions under conditions of high or low reward value, and high or low behavioral effort in male Syrian hamsters. Further, we investigated the role of oxytocin (OT) in a key structure of the mesolimbic reward system, the ventral tegmental area (VTA), in mediating the reinforcing properties of social interaction. Adult male hamsters were placed in a three-chambered apparatus, and allowed access to either a social chamber containing an unrestrained conspecific or a non-social chamber, by pushing through a one-way entry, vertical-swing door. Increasing the duration of social interaction (reward value) decreased the frequency of entering the social interaction chambers, whereas decreasing the duration of social interaction conversely increased the frequency of entries. Moreover, increasing behavioral effort required to access social interaction decreased the frequency of entries, especially under conditions when the duration of social interaction was only 5 s. OT injected into the VTA decreased the frequency of entering social interaction chambers in a manner similar to that observed when duration was increased, whereas injection of an OT receptor antagonist in the VTA increased the frequency of seeking social interaction. Taken together, these data support the hypothesis that activation of OT receptors in the VTA are critical for the reinforcing properties of social interactions. Furthermore, social interactions may exhibit duration and cost dependent reinforcing effects on behavior similar to those observed with food and drugs of abuse.
24S-ketamine exposure in early postnatal period induces social deficit mediated by excessive microglial synaptic pruning.PubMed
Hongyu Zhong, Rou Xue, Yaning Han, et al.
Mol Psychiatry. 2025 Aug;30(8):3615-3631. doi: 10.1038/s41380-025-02949-7. Epub 2025 Mar 11.
The impact of general anesthetics on neurodevelopment is highly controversial in terms of clinical and preclinical studies. Evidence mounted in recent years indicated development of social cognitions was more susceptible to general anesthesia in early life. However, the behavioral characterization during adolescence and underlying mechanisms remains unclear. Herein, we observed that early postnatal S-ketamine exposure specifically induced deficits in sociability and social cognition via a machine learning assistant behavioral analysis toolbox- Social Behavioral Atlas (SBeA). Furthermore, S-ketamine exposure constantly activates microglia in the prefrontal cortex (PFC), mediating excessive synaptic pruning and dendritic structural abnormalities, leading to overexcitation of excitatory synaptic transmission. Notably, S-ketamine exposure activated Stat1-Arg1 pathway in microglia. Downregulating Arg1 expression or prophylactic administrating Arg1 selective inhibitor nor-NOHA could reverse microglial overactivation and attenuate the neurodevelopmental disturbance induced by S-ketamine exposure. Our study identifies the abnormal behavioral phenotypes in adolescence induced by early postnatal S-ketamine exposure and reveals a potential target for preventing anesthesia-related neurodevelopmental abnormalities.
25Oxytocin, motivation and the role of dopamine.PubMed
Tiffany M Love
Pharmacol Biochem Behav. 2014 Apr;119:49-60. doi: 10.1016/j.pbb.2013.06.011. Epub 2013 Jul 9.
The hypothalamic neuropeptide oxytocin has drawn the attention of scientists for more than a century. The understanding of the function of oxytocin has expanded dramatically over the years from a simple peptide adept at inducing uterine contractions and milk ejection to a complex neuromodulator with a capacity to shape human social behavior. Decades of research have outlined oxytocin's ability to enhance intricate social activities ranging from pair bonding, sexual activity, affiliative preferences, and parental behaviors. The precise neural mechanisms underlying oxytocin's influence on such behaviors have just begun to be understood. Research suggests that oxytocin interacts closely with the neural pathways responsible for processing motivationally relevant stimuli. In particular, oxytocin appears to impact dopaminergic activity within the mesocorticolimbic dopamine system, which is crucial not only for reward and motivated behavior but also for the expression of affiliative behaviors. Though most of the work performed in this area has been done using animal models, several neuroimaging studies suggest similar relationships may be observed in humans. In order to introduce this topic further, this paper will review the recent evidence that oxytocin may exert some of its social-behavioral effects through its impact on motivational networks.
26Role of Oxytocin in Different Neuropsychiatric, Neurodegenerative, and Neurodevelopmental Disorders.PubMed
Aya A Ghazy, Omar A Soliman, Aya I Elbahnasi, et al.
Rev Physiol Biochem Pharmacol. 2023;186:95-134. doi: 10.1007/112_2022_72.
Oxytocin has recently gained significant attention because of its role in the pathophysiology and management of dominant neuropsychiatric disorders. Oxytocin, a peptide hormone synthesized in the hypothalamus, is released into different brain regions, acting as a neurotransmitter. Receptors for oxytocin are present in many areas of the brain, including the hypothalamus, amygdala, and nucleus accumbens, which have been involved in the pathophysiology of depression, anxiety, schizophrenia, autism, Alzheimer's disease, Parkinson's disease, and attention deficit hyperactivity disorder. Animal studies have spotlighted the role of oxytocin in social, behavioral, pair bonding, and mother-infant bonding. Furthermore, oxytocin protects fetal neurons against injury during childbirth and affects various behaviors, assuming its possible neuroprotective characteristics. In this review, we discuss some of the concepts and mechanisms related to the role of oxytocin in the pathophysiology and management of some neuropsychiatric, neurodegenerative, and neurodevelopmental disorders.
27Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities.PubMed
Nicole Rigney, Geert J de Vries, Aras Petrulis, et al.
Endocrinology. 2022 Sep 1;163(9). doi: 10.1210/endocr/bqac111.
Oxytocin and vasopressin are peptide hormones secreted from the pituitary that are well known for their peripheral endocrine effects on childbirth/nursing and blood pressure/urine concentration, respectively. However, both peptides are also released in the brain, where they modulate several aspects of social behaviors. Oxytocin promotes maternal nurturing and bonding, enhances social reward, and increases the salience of social stimuli. Vasopressin modulates social communication, social investigation, territorial behavior, and aggression, predominantly in males. Both peptides facilitate social memory and pair bonding behaviors in monogamous species. Here we review the latest research delineating the neural circuitry of the brain oxytocin and vasopressin systems and summarize recent investigations into the circuit-based mechanisms modulating social behaviors. We highlight research using modern molecular genetic technologies to map, monitor activity of, or manipulate neuropeptide circuits. Species diversity in oxytocin and vasopressin effects on social behaviors are also discussed. We conclude with a discussion of the translational implications of oxytocin and vasopressin for improving social functioning in disorders with social impairments, such as autism spectrum disorder.
28Sex, love and oxytocin: Two metaphors and a molecule.PubMed
C Sue Carter
Neurosci Biobehav Rev. 2022 Dec;143:104948. doi: 10.1016/j.neubiorev.2022.104948. Epub 2022 Nov 5.
Dozens of studies, most conducted in the last four decades, have implicated oxytocin, as well as vasopressin and their receptors, in processes that mediate selective sociality and the consequences of early experience. Oxytocin is critical for the capacity to experience emotional safety and healthy sexuality. Oxytocin also plays a central role in almost every aspect of physical and mental health, including the coordination of sociality and loving relationships with physiological reactions to challenges across the lifespan. Species, including prairie voles, that share with humans the capacity for selective social bonds have been a particularly rich source of insights into the behavioral importance of peptides. The purpose of this historical review is to describe the discovery of a central role for oxytocin in behavioral interactions associated with love, and in the capacity to use sociality to anticipate and cope with challenges across the lifespan - a process that here is called "sociostasis."
29Prairie Voles as a Model for Understanding the Genetic and Epigenetic Regulation of Attachment Behaviors.PubMed
Julie M Sadino, Zoe R Donaldson
ACS Chem Neurosci. 2018 Aug 15;9(8):1939-1950. doi: 10.1021/acschemneuro.7b00475. Epub 2018 Apr 6.
Over a lifetime, humans build relationships with family, friends, and partners that are critically important for our mental and physical health. Unlike commonly used laboratory mice and rats, Microtine rodents provide a unique model to study the neurobiology underlying pair bonding and the selective attachments that form between adults. Comparisons between monogamous prairie voles and the closely related but nonmonogamous meadow and montane voles have revealed that brain-region-specific neuropeptide receptor patterning modulates social behavior between and within species. In particular, diversity in vasopressin 1a receptor (V1aR) distribution has been linked to individual and species differences in monogamy-related behaviors such as partner preference, mate guarding, and space use. Given the importance of differential receptor expression for regulating social behavior, a critical question has emerged: What are the genetic and epigenetic mechanisms that underlie brain-region-specific receptor patterns? This review will summarize what is known about how the vasopressin (AVP)-V1aR axis regulates social behaviors via signaling in discrete brain regions. From this work, we propose that brain-region-specific regulatory mechanisms facilitate robust evolvability of V1aR expression to generate diverse sociobehavioral traits. Translationally, we provide a perspective on how these studies have contributed to our understanding of human social behaviors and how brain-region-specific regulatory mechanisms might be harnessed for targeted therapies to treat social deficits in psychiatric disorders such as depression, complicated grief, and autism spectrum disorder.
30The neurobiology of pair bonding: insights from a socially monogamous rodent.PubMed
Kimberly A Young, Kyle L Gobrogge, Yan Liu, et al.
Front Neuroendocrinol. 2011 Jan;32(1):53-69. doi: 10.1016/j.yfrne.2010.07.006. Epub 2010 Aug 3.
The formation of enduring relationships between adult mates (i.e., pair bonds) is an integral aspect of human social behavior and has been implicated in both physical and psychological health. However, due to the inherent complexity of these bonds and the relative rarity with which they are formed in other mammalian species, we know surprisingly little about their underlying neurobiology. Over the past few decades, the prairie vole (Microtus ochrogaster) has emerged as an animal model of pair bonding. Research in this socially monogamous rodent has provided valuable insight into the neurobiological mechanisms that regulate pair bonding behaviors. Here, we review these studies and discuss the neural regulation of three behaviors inherent to pair bonding: the formation of partner preferences, the subsequent development of selective aggression toward unfamiliar conspecifics, and the bi-parental care of young. We focus on the role of vasopressin, oxytocin, and dopamine in the regulation of these behaviors, but also discuss the involvement of other neuropeptides, neurotransmitters, and hormones. These studies may not only contribute to the understanding of pair bonding in our own species, but may also offer insight into the underlying causes of social deficits noted in several mental health disorders.
31Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin.PubMed
Gül Dölen, Ayeh Darvishzadeh, Kee Wui Huang, et al.
Nature. 2013 Sep 12;501(7466):179-84. doi: 10.1038/nature12518.
Social behaviours in species as diverse as honey bees and humans promote group survival but often come at some cost to the individual. Although reinforcement of adaptive social interactions is ostensibly required for the evolutionary persistence of these behaviours, the neural mechanisms by which social reward is encoded by the brain are largely unknown. Here we demonstrate that in mice oxytocin acts as a social reinforcement signal within the nucleus accumbens core, where it elicits a presynaptically expressed long-term depression of excitatory synaptic transmission in medium spiny neurons. Although the nucleus accumbens receives oxytocin-receptor-containing inputs from several brain regions, genetic deletion of these receptors specifically from dorsal raphe nucleus, which provides serotonergic (5-hydroxytryptamine; 5-HT) innervation to the nucleus accumbens, abolishes the reinforcing properties of social interaction. Furthermore, oxytocin-induced synaptic plasticity requires activation of nucleus accumbens 5-HT1B receptors, the blockade of which prevents social reward. These results demonstrate that the rewarding properties of social interaction in mice require the coordinated activity of oxytocin and 5-HT in the nucleus accumbens, a mechanistic insight with implications for understanding the pathogenesis of social dysfunction in neuropsychiatric disorders such as autism.
32Modulating the Neuromodulators: Dopamine, Serotonin, and the Endocannabinoid System.PubMed
Kate Z Peters, Joseph F Cheer, Raffaella Tonini
Trends Neurosci. 2021 Jun;44(6):464-477. doi: 10.1016/j.tins.2021.02.001. Epub 2021 Mar 3.
Dopamine (DA), serotonin (5-hydroxytryptamine, 5-HT), and endocannabinoids (ECs) are key neuromodulators involved in many aspects of motivated behavior, including reward processing, reinforcement learning, and behavioral flexibility. Among the longstanding views about possible relationships between these neuromodulators is the idea of DA and 5-HT acting as opponents. This view has been challenged by emerging evidence that 5-HT supports reward seeking via activation of DA neurons in the ventral tegmental area. Adding an extra layer of complexity to these interactions, the endocannabinoid system is uniquely placed to influence dopaminergic and serotonergic neurotransmission. In this review we discuss how these three neuromodulatory systems interact at the cellular and circuit levels. Technological advances that facilitate precise identification and control of genetically targeted neuronal populations will help to achieve a better understanding of the complex relationship between these essential systems, and the potential relevance for motivated behavior.
33Estrogen Control of Social Behaviors.PubMed
Oluwadamilola O Lawal, Dayu Lin, Julieta E Lischinsky
Annu Rev Neurosci. 2025 Jul;48(1):125-147. doi: 10.1146/annurev-neuro-112723-041639. Epub 2025 Feb 21.
Social behaviors, including parental care, mating, and fighting, all depend on the hormonal milieu of an organism. Decades of work highlighted estrogen as a key hormonal controller of social behaviors, exerting its influence primarily through binding to estrogen receptor alpha (ERα). Recent technological advances in chemogenetics, optogenetics, gene editing, and transgenic model organisms have allowed for a detailed understanding of the neuronal subpopulations and circuits for estrogen action across -expressing interconnected brain regions. Focusing on rodent studies, in this review we examine classical and contemporary research demonstrating the multifaceted role of estrogen and ERα in regulating social behaviors in a sex-specific and context-dependent manner. We highlight gaps in knowledge, particularly a missing link in the molecular cascade that allows estrogen to exert such a diverse behavioral repertoire through the coordination of gene expression changes. Understanding the molecular and cellular basis of ERα's action in social behaviors provides insights into the broader mechanisms of hormone-driven behavior modulation across the lifespan.
34Hormonal and circuit mechanisms controlling female sexual behavior.PubMed
Sayaka Inoue
Front Neural Circuits. 2024 May 1;18:1409349. doi: 10.3389/fncir.2024.1409349. eCollection 2024.
Sexual behavior is crucial for reproduction in many animals. In many vertebrates, females exhibit sexual behavior only during a brief period surrounding ovulation. Over the decades, studies have identified the roles of ovarian sex hormones, which peak in levels around the time of ovulation, and the critical brain regions involved in the regulation of female sexual behavior. Modern technical innovations have enabled a deeper understanding of the neural circuit mechanisms controlling this behavior. In this review, I summarize our current knowledge and discuss the neural circuit mechanisms by which female sexual behavior occurs in association with the ovulatory phase of their cycle.
35Integrating reproductive states and social cues in the control of sociosexual behaviors.PubMed
Yuping Wang, Xinli Song, Xiangmao Chen, et al.
Cell. 2025 Jun 26;188(13):3530-3549.e24. doi: 10.1016/j.cell.2025.04.035. Epub 2025 May 20.
Female sociosexual behaviors, essential for survival and reproduction, are modulated by ovarian hormones and triggered in the context of appropriate social cues. Here, we identify primary estrous-sensitive Cacna1h-expressing medial prefrontal cortex (mPFC) neurons that integrate hormonal states with recognition of potential mates to orchestrate these complex cognitive behaviors. Bidirectional manipulation of mPFC neurons shifts opposite-sex-directed social behaviors between estrus and diestrus females via anterior hypothalamic outputs. In males, these neurons serve opposite functions compared with estrus females. Miniscope imaging reveals mixed representation of self-estrous states and social target sex in distinct mPFC subpopulations, with biased encoding of opposite-sex cues in estrus females and males. Mechanistically, ovarian-hormone-induced Cacna1h upregulation enhances T-type rebound excitation after oxytocin inhibition, driving estrus-specific activity changes and the sexually dimorphic function of mPFC neurons. These findings uncover a prefrontal circuit that integrates internal hormonal states and target-sex information to exert sexually bivalent top-down control over adaptive social behaviors.
36Hormonal regulation of social ascent and temporal patterns of behavior in an African cichlid.PubMed
Beau A Alward, Austin T Hilliard, Ryan A York, et al.
Horm Behav. 2019 Jan;107:83-95. doi: 10.1016/j.yhbeh.2018.12.010. Epub 2019 Jan 4.
For many species, social rank determines which individuals perform certain social behaviors and when. Higher ranking or dominant (DOM) individuals maintain status through aggressive interactions and perform courtship behaviors while non-dominant (ND) individuals do not. In some species ND individuals ascend (ASC) in social rank when the opportunity arises. Many important questions related to the mechanistic basis of social ascent remain to be answered. We probed whether androgen signaling regulates social ascent in male Astatotilapia burtoni, an African cichlid whose social hierarchy can be readily controlled in the laboratory. As expected, androgen receptor (AR) antagonism abolished reproductive behavior during social ascent. However, we discovered multiple AR- and status-dependent temporal behavioral patterns that typify social ascent and dominance. AR antagonism in ASC males increased the time between successive behaviors compared to DOM males. Socially ascending males, independent of AR activation, were more likely than DOM males to follow aggressive displays with another aggressive display. Further analyses revealed differences in the sequencing of aggressive and courtship behaviors, wherein DOM males were more likely than ASC males to follow male-directed aggression with courtship displays. Strikingly, this difference was driven mostly by ASC males taking longer to transition from aggression to courtship, suggesting ASC males can perform certain DOM-typical temporal behavioral patterns. Our results indicate androgen signaling is necessary for social ascent and hormonal signaling and social experience may shape the full suite of DOM-typical behavioral patterns.
37Endocrine and neuroendocrine regulation of social status in cichlid fishes.PubMed
Karen P Maruska, Chase M Anselmo, Teisha King, et al.
Horm Behav. 2022 Mar;139:105110. doi: 10.1016/j.yhbeh.2022.105110. Epub 2022 Jan 19.
Position in a dominance hierarchy profoundly impacts group members' survival, health, and reproductive success. Thus, understanding the mechanisms that regulate or are associated with an individuals' social position is important. Across taxa, various endocrine and neuroendocrine signaling systems are implicated in the control of social rank. Cichlid fishes, with their often-limited resources of food, shelter, and mates that leads to competition, have provided important insights on the proximate and ultimate mechanisms related to establishment and maintenance of dominance hierarchies. Here we review the existing information on the relationships between endocrine (e.g., circulating hormones, gonadal and other tissue measures) and neuroendocrine (e.g., central neuropeptides, biogenic amines, steroids) systems and dominant and subordinate social rank in male cichlids. Much of the current literature is focused on only a few representative cichlids, particularly the African Astatotilapia burtoni, and several other African and Neotropical species. Many hormonal regulators show distinct differences at multiple biological levels between dominant and subordinate males, but generalizations are complicated by variations in experimental paradigms, methodological approaches, and in the reproductive and parental care strategies of the study species. Future studies that capitalize on the diversity of hierarchical structures among cichlids should provide insights towards better understanding the endocrine and neuroendocrine mechanisms contributing to social rank. Further, examination of this topic in cichlids will help reveal the selective pressures driving the evolution of endocrine-related phenotypic traits that may facilitate an individual's ability to acquire and maintain a specific social rank to improve survival and reproductive success.
38Sex Differences in Social Cognition.PubMed
Pietro Paletta, Noah Bass, Dario Aspesi, et al.
Curr Top Behav Neurosci. 2023;62:207-234. doi: 10.1007/7854_2022_325.
In this review we explore the sex differences underlying various types of social cognition. Particular focus will be placed on the behaviors of social recognition, social learning, and aggression. Known similarities and differences between sexes in the expressions of these behaviors and the known brain regions where these behaviors are mediated are discussed. The role that the sex hormones (estrogens and androgens) have as well as possible interactions with other neurochemicals, such as oxytocin, vasopressin, and serotonin is reviewed as well. Finally, implications about these findings on the mediation of social cognition are mediated and the sex differences related to humans are considered.
39Species, sex and individual differences in the vasotocin/vasopressin system: relationship to neurochemical signaling in the social behavior neural network.PubMed
H Elliott Albers
Front Neuroendocrinol. 2015 Jan;36:49-71. doi: 10.1016/j.yfrne.2014.07.001. Epub 2014 Aug 4.
Arginine-vasotocin (AVT)/arginine vasopressin (AVP) are members of the AVP/oxytocin (OT) superfamily of peptides that are involved in the regulation of social behavior, social cognition and emotion. Comparative studies have revealed that AVT/AVP and their receptors are found throughout the "social behavior neural network (SBNN)" and display the properties expected from a signaling system that controls social behavior (i.e., species, sex and individual differences and modulation by gonadal hormones and social factors). Neurochemical signaling within the SBNN likely involves a complex combination of synaptic mechanisms that co-release multiple chemical signals (e.g., classical neurotransmitters and AVT/AVP as well as other peptides) and non-synaptic mechanisms (i.e., volume transmission). Crosstalk between AVP/OT peptides and receptors within the SBNN is likely. A better understanding of the functional properties of neurochemical signaling in the SBNN will allow for a more refined examination of the relationships between this peptide system and species, sex and individual differences in sociality.
40A review of the effects of different types of social behaviors on the recruitment of neuropeptides and neurotransmitters in the nucleus accumbens.PubMed
Johnathan M Borland
Front Neuroendocrinol. 2025 Apr;77:101175. doi: 10.1016/j.yfrne.2025.101175. Epub 2025 Jan 31.
There is a lack of understanding of the neural mechanisms regulating the rewarding effects of social interactions. A significant contributor to this lack of clarity is the diversity of social behaviors and animal models utilized to investigate mechanisms. Other sources of the lack of clarity are the diversity of brain regions that can regulate social reward and the diversity of signaling pathways that regulate reward. To provide some clarity into the mechanisms of social reward, this review focused on the brain region most implicated in reward for multiple stimuli, the nucleus accumbens, and surveyed (systematically reviewed) studies that investigated the relationship between social interaction and five signaling systems implicated in the regulation of reward and social behavior: oxytocin, vasopressin, serotonin, opioids and endocannabinoids. Moreover, all of these studies were organized by the type of social behavior studied: affiliative interactions, play behavior, aggression, social defeat, sex behavior, pair-bonding, parental behavior and social isolation. From this survey and organization, this review concludes that oxytocin, endocannabinoids and mu-opioid receptors in the nucleus accumbens positively regulate the rewarding social behaviors, and kappa-opioid receptors negatively regulate the rewarding social behaviors. The opposite profile is observed for these signaling systems for the aversive social behaviors. More studies are needed to investigate the directional role of the serotonin system in the nucleus accumbens in the regulation of many types of social behaviors, and vasopressin likely does not act in the nucleus accumbens in the regulation of the valence of social behaviors. Many of these different signaling systems are also interdependent of one another in the regulation of different types of social behaviors. Finally, the interaction of these signaling systems with dopamine in the nucleus accumbens is briefly discussed.
41An Overview of the Main Genetic, Epigenetic and Environmental Factors Involved in Autism Spectrum Disorder Focusing on Synaptic Activity.PubMed
Elena Masini, Eleonora Loi, Ana Florencia Vega-Benedetti, et al.
Int J Mol Sci. 2020 Nov 5;21(21):8290. doi: 10.3390/ijms21218290.
Autism spectrum disorder (ASD) is a neurodevelopmental disorder that affects social interaction and communication, with restricted interests, activity and behaviors. ASD is highly familial, indicating that genetic background strongly contributes to the development of this condition. However, only a fraction of the total number of genes thought to be associated with the condition have been discovered. Moreover, other factors may play an important role in ASD onset. In fact, it has been shown that parental conditions and in utero and perinatal factors may contribute to ASD etiology. More recently, epigenetic changes, including DNA methylation and micro RNA alterations, have been associated with ASD and proposed as potential biomarkers. This review aims to provide a summary of the literature regarding ASD candidate genes, mainly focusing on synapse formation and functionality and relevant epigenetic and environmental aspects acting in concert to determine ASD onset.
42Anterior cingulate cortex parvalbumin and somatostatin interneurons shape social behavior in male mice.PubMed
Chuchu Qi, Wenqi Sima, Honghui Mao, et al.
Nat Commun. 2025 May 4;16(1):4156. doi: 10.1038/s41467-025-59473-z.
The anterior cingulate cortex (ACC) is essential for social behavior, and its dysfunction is implicated in social interaction deficits in autism. Pyramidal neuron activity in the ACC is modulated by parvalbumin (PV) and somatostatin (SST) interneurons, though their specific roles in social interactions remain unclear. Here, we demonstrate that PV and SST interneurons differentially contribute to the regulation of social interactions. In a Shank3-deficient autistic model, the expression of Kcnh7, a risk gene for autism, is reduced in both PV and SST interneurons. Knocking out Kcnh7 in either interneuron subtype leads to social interaction deficits. Furthermore, projections from the lateral posterior thalamic nucleus (mediorostral part, LPMR) to PV interneurons and from the ventral hippocampus (vHPC) to SST interneurons differentially modulate social interactions. These findings provide new insights into the distinct roles of PV and SST interneurons in social processes and their contributions to autism-related pathophysiology.
43Aralar Sequesters GABA into Hyperactive Mitochondria, Causing Social Behavior Deficits.PubMed
Alexandros K Kanellopoulos, Vittoria Mariano, Marco Spinazzi, et al.
Cell. 2020 Mar 19;180(6):1178-1197.e20. doi: 10.1016/j.cell.2020.02.044.
Social impairment is frequently associated with mitochondrial dysfunction and altered neurotransmission. Although mitochondrial function is crucial for brain homeostasis, it remains unknown whether mitochondrial disruption contributes to social behavioral deficits. Here, we show that Drosophila mutants in the homolog of the human CYFIP1, a gene linked to autism and schizophrenia, exhibit mitochondrial hyperactivity and altered group behavior. We identify the regulation of GABA availability by mitochondrial activity as a biologically relevant mechanism and demonstrate its contribution to social behavior. Specifically, increased mitochondrial activity causes gamma aminobutyric acid (GABA) sequestration in the mitochondria, reducing GABAergic signaling and resulting in social deficits. Pharmacological and genetic manipulation of mitochondrial activity or GABA signaling corrects the observed abnormalities. We identify Aralar as the mitochondrial transporter that sequesters GABA upon increased mitochondrial activity. This study increases our understanding of how mitochondria modulate neuronal homeostasis and social behavior under physiopathological conditions.
44The role of monoamine oxidase A in the neurobiology of aggressive, antisocial, and violent behavior: A tale of mice and men.PubMed
Nathan J Kolla, Marco Bortolato
Prog Neurobiol. 2020 Nov;194:101875. doi: 10.1016/j.pneurobio.2020.101875. Epub 2020 Jun 20.
Over the past two decades, research has revealed that genetic factors shape the propensity for aggressive, antisocial, and violent behavior. The best-documented gene implicated in aggression is MAOA (Monoamine oxidase A), which encodes the key enzyme for the degradation of serotonin and catecholamines. Congenital MAOA deficiency, as well as low-activity MAOA variants, has been associated with a higher risk for antisocial behavior (ASB) and violence, particularly in males with a history of child maltreatment. Indeed, the interplay between low MAOA genetic variants and early-life adversity is the best-documented gene × environment (G × E) interaction in the pathophysiology of aggression and ASB. Additional evidence indicates that low MAOA activity in the brain is strongly associated with a higher propensity for aggression; furthermore, MAOA inhibition may be one of the primary mechanisms whereby prenatal smoke exposure increases the risk of ASB. Complementary to these lines of evidence, mouse models of Maoa deficiency and G × E interactions exhibit striking similarities with clinical phenotypes, proving to be valuable tools to investigate the neurobiological mechanisms underlying antisocial and aggressive behavior. Here, we provide a comprehensive overview of the current state of the knowledge on the involvement of MAOA in aggression, as defined by preclinical and clinical evidence. In particular, we show how the convergence of human and animal research is proving helpful to our understanding of how MAOA influences antisocial and violent behavior and how it may assist in the development of preventative and therapeutic strategies for aggressive manifestations.
45Epigenetic Regulation of the Social Brain.PubMed
Anna Bludau, Melanie Royer, Gunter Meister, et al.
Trends Neurosci. 2019 Jul;42(7):471-484. doi: 10.1016/j.tins.2019.04.001. Epub 2019 May 15.
Social behavior, a highly adaptive and crucial component of mammalian life, is regulated by particularly sensitive regulatory brain mechanisms. Substantial evidence implicates classical epigenetic mechanisms including histone modifications, DNA methylation, and nucleosome remodeling as well as nonclassical mechanisms mediated by noncoding RNA in the regulation of social behavior. These mechanisms collectively form the 'epigenetic network' that orchestrates genomic integration of salient and transient social experiences. Consequently, its dysregulation has been linked to behavioral deficits and psychopathologies. This review focuses on the role of the epigenetic network in regulating the enduring effects of social experiences during early-life, adolescence, and adulthood. We discuss research in animal models, primarily rodents, and associations between dysregulation of epigenetic mechanisms and human psychopathologies, specifically autism spectrum disorder (ASD) and schizophrenia.
46Mechanisms of stress in the brain.PubMed
Bruce S McEwen, Nicole P Bowles, Jason D Gray, et al.
Nat Neurosci. 2015 Oct;18(10):1353-63. doi: 10.1038/nn.4086. Epub 2015 Sep 25.
The brain is the central organ involved in perceiving and adapting to social and physical stressors via multiple interacting mediators, from the cell surface to the cytoskeleton to epigenetic regulation and nongenomic mechanisms. A key result of stress is structural remodeling of neural architecture, which may be a sign of successful adaptation, whereas persistence of these changes when stress ends indicates failed resilience. Excitatory amino acids and glucocorticoids have key roles in these processes, along with a growing list of extra- and intracellular mediators that includes endocannabinoids and brain-derived neurotrophic factor (BDNF). The result is a continually changing pattern of gene expression mediated by epigenetic mechanisms involving histone modifications and CpG methylation and hydroxymethylation as well as by the activity of retrotransposons that may alter genomic stability. Elucidation of the underlying mechanisms of plasticity and vulnerability of the brain provides a basis for understanding the efficacy of interventions for anxiety and depressive disorders as well as age-related cognitive decline.
47Physical exercise mediates cortical synaptic protein lactylation to improve stress resilience.PubMed
Lan Yan, Yajie Wang, Haidong Hu, et al.
Cell Metab. 2024 Sep 3;36(9):2104-2117.e4. doi: 10.1016/j.cmet.2024.07.018. Epub 2024 Aug 19.
Lactate is a critical metabolite during the body's adaption to exercise training, which effectively relieves anxiety-like disorders. The biological mechanism of lactate in the exercise-mediated anxiolytic effect has, however, not been comprehensively investigated. Here, we report that exercise-induced lactate markedly potentiates the lactylation of multiple synaptic proteins, among which synaptosome-associated protein 91 (SNAP91) is the critical molecule for synaptic functions. Both anatomical evidence and in vivo recording data showed that the lactylation of SNAP91 confers resilience against chronic restraint stress (CRS) via potentiating synaptic structural formation and neuronal activity in the medial prefrontal cortex (mPFC). More interestingly, exercise-potentiated lactylation of SNAP91 is necessary for the prevention of anxiety-like behaviors in CRS mice. These results collectively suggest a previously unrecognized non-histone lactylation in the brain for modulating mental functions and provide evidence for the brain's metabolic adaption during exercise paradigms.
48Epigenetic programming by maternal behavior.PubMed
Ian C G Weaver, Nadia Cervoni, Frances A Champagne, et al.
Nat Neurosci. 2004 Aug;7(8):847-54. doi: 10.1038/nn1276. Epub 2004 Jun 27.
Here we report that increased pup licking and grooming (LG) and arched-back nursing (ABN) by rat mothers altered the offspring epigenome at a glucocorticoid receptor (GR) gene promoter in the hippocampus. Offspring of mothers that showed high levels of LG and ABN were found to have differences in DNA methylation, as compared to offspring of 'low-LG-ABN' mothers. These differences emerged over the first week of life, were reversed with cross-fostering, persisted into adulthood and were associated with altered histone acetylation and transcription factor (NGFI-A) binding to the GR promoter. Central infusion of a histone deacetylase inhibitor removed the group differences in histone acetylation, DNA methylation, NGFI-A binding, GR expression and hypothalamic-pituitary-adrenal (HPA) responses to stress, suggesting a causal relation among epigenomic state, GR expression and the maternal effect on stress responses in the offspring. Thus we show that an epigenomic state of a gene can be established through behavioral programming, and it is potentially reversible.
49Stress, microRNAs, and stress-related psychiatric disorders: an overview.PubMed
Laura Musazzi, Jessica Mingardi, Alessandro Ieraci, et al.
Mol Psychiatry. 2023 Dec;28(12):4977-4994. doi: 10.1038/s41380-023-02139-3. Epub 2023 Jun 30.
Stress is a major risk factor for psychiatric disorders. During and after exposure to stressors, the stress response may have pro- or maladaptive consequences, depending on several factors related to the individual response and nature of the stressor. However, the mechanisms mediating the long-term effects of exposure to stress, which may ultimately lead to the development of stress-related disorders, are still largely unknown. Epigenetic mechanisms have been shown to mediate the effects of the environment on brain gene expression and behavior. MicroRNAs, small non-coding RNAs estimated to control the expression of about 60% of all genes by post-transcriptional regulation, are a fundamental epigenetic mechanism. Many microRNAs are expressed in the brain, where they work as fine-tuners of gene expression, with a key role in the regulation of homeostatic balance, and a likely influence on pro- or maladaptive brain changes. Here we have selected a number of microRNAs, which have been strongly implicated as mediators of the effects of stress in the brain and in the development of stress-related psychiatric disorders. For all of them recent evidence is reported, obtained from rodent stress models, manipulation of microRNAs levels with related behavioral changes, and clinical studies of stress-related psychiatric disorders. Moreover, we have performed a bioinformatic analysis of the predicted brain-expressed target genes of the microRNAs discussed, and found a central role for mechanisms involved in the regulation of synaptic function. The complex regulatory role of microRNAs has suggested their use as biomarkers for diagnosis and treatment response, as well as possible therapeutic drugs. While, microRNA-based diagnostics have registered advancements, particularly in oncology and other fields, and many biotech companies have launched miRNA therapeutics in their development pipeline, the development of microRNA-based tests and drugs for brain disorders is comparatively slower.
50Gene-environment interaction and suicidal behavior.PubMed
Alec Roy, Marco Sarchiopone, Vladimir Carli
J Psychiatr Pract. 2009 Jul;15(4):282-8. doi: 10.1097/01.pra.0000358314.88931.b5.
Studies have increasingly shown that gene-environment interactions are important in psychiatry. Suicidal behavior is a major public health problem. Suicide is generally considered to be a multi-determined act involving various areas of proximal and distal risk. Genetic risk factors are estimated to account for approximately 30% to 40% of the variance in suicidal behavior. In this article, the authors review relevant studies concerning the interaction between the serotonin transporter gene and environmental variables as a model of gene-environment interactions that may have an impact on suicidal behavior. The findings reviewed here suggest that there may be meaningful interactions between distal and proximal suicide risk factors that may amplify the risk of suicidal behavior. Future studies of suicidal behavior should examine both genetic and environmental variables and examine for gene-environment interactions.
51Neurocriminology.PubMed
Benjamin R Nordstrom, Yu Gao, Andrea L Glenn, et al.
Adv Genet. 2011;75:255-83. doi: 10.1016/B978-0-12-380858-5.00006-X.
In the past several decades there has been an explosion of research into the biological correlates to antisocial behavior. This chapter reviews the state of current research on the topic, including a review of the genetics, neuroimaging, neuropsychological, and electrophysiological studies in delinquent and antisocial populations. Special attention is paid to the biopsychosocial model and gene-environment interactions in producing antisocial behavior.
52Stress, epigenetics and depression: A systematic review.PubMed
Caroline Park, Joshua D Rosenblat, Elisa Brietzke, et al.
Neurosci Biobehav Rev. 2019 Jul;102:139-152. doi: 10.1016/j.neubiorev.2019.04.010. Epub 2019 Apr 18.
Environmental stressors, such as childhood maltreatment, have been recognized to contribute to the development of depression. Growing evidence suggests that epigenetic changes are a key mechanism by which stressors interact with the genome leading to stable changes in DNA structure, gene expression, and behaviour. The current review aimed to evaluate the relationship between stress-associated epigenetic changes and depression. Human studies were identified via systematic searching of PubMed/Medline from inception to February 2018. Seventeen articles were identified. Stress-associated epigenetic changes in the following genes were correlated with depression: NRC31, SLCA4, BDNF, FKBP5, SKA2, OXTR, LINGO3, POU3F1 and ITGB1. Epigenetic changes in glucocorticoid signaling (e.g., NR3C1, FKBP5), serotonergic signaling (e.g. SLC6A4), and neurotrophin (e.g., BDNF) genes appear to be the most promising therapeutic targets for future research. However, continued research is warranted due to inconsistent findings regarding the directionality of epigenetic modification. Future studies should also aim to control for the use of psychotropic agents due to their widespread use in depressed populations and established effects on DNA methylation.
53Oxytocin and Anxiety Disorders.PubMed
Michael G Gottschalk, Katharina Domschke
Curr Top Behav Neurosci. 2018;35:467-498. doi: 10.1007/7854_2017_25.
In the present chapter, we review the literature focusing on oxytocin (OT)-centered research in anxiety spectrum conditions, comprising separation anxiety disorder, specific phobias, social anxiety disorder (SAD), panic disorder, generalized anxiety disorder, and anxiety-related endophenotypes (e.g., trust behavior, behavioral inhibition, neuroticism, and state/trait anxiety). OT receptor gene (OXTR) polymorphisms have been implicated in gene-environment interactions with attachment style and childhood maltreatment and to influence clinical outcomes, including SAD intensity and limbic responsiveness. Epigenetic OXTR DNA methylation patterns have emerged as a link between categorical, dimensional, neuroendocrinological, and neuroimaging SAD correlates, highlighting them as potential peripheral surrogates of the central oxytocinergic tone. A pathophysiological framework of OT integrating the dynamic nature of epigenetic biomarkers and the summarized genetic and peripheral evidence is proposed. Finally, we emphasize opportunities and challenges of OT as a key network node of social interaction and fear learning in social contexts. In conjunction with multi-level investigations incorporating a dimensional understanding of social affiliation and avoidance in anxiety spectrum disorders, these concepts will help to promote research for diagnostic, state, and treatment response biomarkers of the OT system, advancing towards indicated preventive interventions and personalized treatment approaches.
54Laparotomy and burst suppression-inducing sevoflurane induce subtle long-term changes in anxiety and social behavior in late postnatal mice.PubMed
Tao Zhang, Yulim Lee, Xianshu Ju, et al.
Korean J Anesthesiol. 2025 Aug;78(4):382-394. doi: 10.4097/kja.24768. Epub 2025 Apr 9.
BACKGROUND: Despite strong preclinical evidence, clinical studies have reported minimal effects of early anesthesia on neurodevelopment. This discrepancy may be due to limitations of preclinical studies, including the absence of clear criteria for appropriate anesthetic depth, lack of physiological monitoring, and absence of a surgical insult. Therefore, we aimed to evaluate the effects of sevoflurane in a more clinically relevant setting by addressing these known limitations. METHODS: After confirming robust burst suppression (BS) at 2.5% sevoflurane, postnatal day 17 (PND17) mice were assigned to three groups: a Control group, no intervention; BS (-) group, surgery with 1.4% sevoflurane; and a BS (+) group, surgery with 1.4%-2.5% sevoflurane. Total duration of anesthesia was 2 h, and blood pressure was non-invasively measured in a subset of mice. Long-term behavioral changes were evaluated from PND56 to PND62 at a two-day interval. RESULTS: We found subtle but significant changes in anxiety and sociability only in BS (+) group mice. Change in anxiety level was observed in the light/dark box test, with the number of transitions between chambers significantly lower in the BS (+) group (P = 0.025). Reduced sociability was observed in the three-chamber test, as mice in the BS (+) group did not significantly prefer the chamber containing a stranger mouse (P = 0.065). CONCLUSIONS: Both surgery and excessive anesthesia depth are necessary to induce subtle yet long-term behavioral changes in young mice. Future preclinical studies should reconsider sevoflurane concentration and account for surgical trauma as a significant factor when investigating anesthesia-induced neurotoxicity.
55Maternal deprivation affects goat kids' social behavior before and after weaning.PubMed
Claire Toinon, Susanne Waiblinger, Jean-Loup Rault
Dev Psychobiol. 2022 May;64(4):e22269. doi: 10.1002/dev.22269.
Maternal deprivation has been shown to disrupt the development of neonates. Nevertheless, separating the young animals from their dams soon after birth is a common practice in dairy farming. We investigated the effects of maternal deprivation on goat kids' (Capra hircus) social behavior and social ontogeny before and after weaning. Twenty female kids were raised together with their dams (DR kids) and other lactating goats and kids, whereas 20 female kids were separated from their dams 3 days after birth and artificially reared together (AR kids). At weaning, each treatment group was split in half and moved into two new pens where they were mixed with the other treatment group. Social behaviors were recorded before and after weaning. Before weaning, AR kids were observed performing more play-fighting, racing, stepping on each other, and standing in contact with each other than DR kids, but AR allogroomed less and spent less time resting alone than DR kids. After weaning and mixing of the treatments, DR kids initiated more and received less agonistic interactions than AR kids, but this difference reduced across the 5 weeks of observations as AR kids appeared to progressively change their social behavior after interacting with DR kids.
56Long-term effects of early maternal deprivation on goat social behaviour.PubMed
C Toinon, S Waiblinger, R Palme, et al.
Animal. 2023 May;17(5):100814. doi: 10.1016/j.animal.2023.100814. Epub 2023 Apr 17.
Early maternal deprivation has been shown to disrupt goat kids' social behaviour and stress-coping strategy, and has long-term effects in other species like cattle. We studied the long-term effects of early maternal deprivation on 18-month-old goats. Seventeen goats were raised together with their dams (DR kids) and other lactating goats and kids, while 18 goats were separated from their dams three days after birth and artificially reared together (AR kids). Kids of both treatments were weaned around two to three months of age, grouped and raised together until this study 15 months later. Affiliative, playful, and agonistic behaviour was recorded by focal sampling in the home pen, when the focal goat had rejoined the herd after being physically isolated for 3 minutes, and after the focal goat was restrained and manipulated for 3 minutes. Behavioural observations were also conducted after the goats were introduced in groups of four in a herd of 77 unknown, lactating multiparous goats. Avoidance distance tests were performed in the home pen to assess the human-animal relationship. Salivary cortisol was measured before and after physical isolation, and faecal glucocorticoid metabolites were measured before and 24 hours after introduction in the lactating herd. In the home pen, AR goats were involved in less head nudging than DR goats, but other social behaviours or their behavioural and physiological response to the various stressful situations were not affected by their rearing treatment. Upon introduction in a DR lactating herd, most of the agonistic interactions observed were initiated by multiparous goats towards the introduced AR and DR goats alike. AR goats received more threats from the multiparous goats than DR goats, but were involved in less clashing than DR goats. AR goats showed less avoidance of familiar and unfamiliar humans than DR goats. Overall, previously AR and DR goats showed only a few differences in affiliative and agonistic behaviours in their home pen or after being exposed to different stressors 15 months later. Nonetheless, after being introduced into a multiparous goat herd, AR goats were still threatened more often than DR goats, and DR goats clashed more than AR goats, suggesting some persistent differences in their social abilities observed at an early age before and after weaning. As predicted, AR goats remained less fearful of humans than DR goats.
57Altered corticosterone levels and social play behavior after prolonged maternal separation in adolescent male but not female Wistar rats.PubMed
Stina Lundberg, My Martinsson, Ingrid Nylander, et al.
Horm Behav. 2017 Jan;87:137-144. doi: 10.1016/j.yhbeh.2016.11.016. Epub 2016 Nov 22.
Early-life socio-environmental factors are crucial for normal developmental processes; adverse experiences early in life can therefore lead to detrimental effects in several physiological systems. The aim of this study was to examine short-term effects of early adverse experiences in a maternal separation (MS) rodent model. In this study two separation conditions were used: daily 15- (MS15) or 360-min (MS360) separation of the litter from the dam during postnatal day 1-21. In early adolescence, male and female offspring were subjected to a single-isolation procedure with analysis of corticosterone levels prior to and after isolation. In addition, social play behavior was assessed during mid-adolescence. There was a clear difference between male and female offspring in both tests performed. There was no difference in corticosterone levels between the female MS groups, whereas MS360 males showed higher baseline and recovery corticosterone levels than MS15 males. The amount of pinning, a specific social play behavior, was affected by rearing with MS360 males having a higher frequency than MS15 males, while there was no difference between the female MS groups. The observation that males but not females are affected by MS360 has previously been reported for adult animals, and herein we show that this difference is present already in adolescence. Changes in corticosterone levels and social behavior following early-life adversity have been associated with adult behavioral alterations, and our results confirm that these changes emerge already within adolescence.
58Oxytocin neurons mediate the effect of social isolation via the VTA circuits.PubMed
Stefano Musardo, Alessandro Contestabile, Marit Knoop, et al.
Elife. 2022 Apr 22;11:e73421. doi: 10.7554/eLife.73421.
Social interaction during adolescence strongly influences brain function and behavior, and the recent pandemic has emphasized the devastating effect of social distancing on mental health. While accumulating evidence has shown the importance of the reward system in encoding specific aspects of social interaction, the consequences of social isolation on the reward system and the development of social skills later in adulthood are still largely unknown. Here, we found that 1 week of social isolation during adolescence in male mice increased social interaction at the expense of social habituation and social novelty preference. Behavioral changes were accompanied by the acute hyperexcitability of putative dopamine (pDA) neurons in the ventral tegmental area and long-lasting expression of GluA2-lacking AMPARs at excitatory inputs onto pDA neurons that project to the prefrontal cortex. Social isolation-dependent behavioral deficits and changes in neural activity and synaptic plasticity were reversed by chemogenetic inhibition of oxytocin neurons in the paraventricular nucleus of the hypothalamus. These results demonstrate that social isolation in male mice has acute and long-lasting effects on social interaction and suggest that homeostatic adaptations mediate these effects within the reward circuit.
59A developmental social neuroscience model for understanding loneliness in adolescence.PubMed
Nichol M L Wong, Patcy P S Yeung, Tatia M C Lee
Soc Neurosci. 2018 Feb;13(1):94-103. doi: 10.1080/17470919.2016.1256832. Epub 2016 Nov 18.
Loneliness is prevalent in adolescents. Although it can be a normative experience, children and adolescents who experience loneliness are often at risk for anxiety, depression, and suicide. Research efforts have been made to identify the neurobiological basis of such distressful feelings in our social brain. In adolescents, the social brain is still undergoing significant development, which may contribute to their increased and differential sensitivity to the social environment. Many behavioral studies have shown the significance of attachment security and social skills in adolescents' interactions with the social world. In this review, we propose a developmental social neuroscience model that extends from the social neuroscience model of loneliness. In particular, we argue that the social brain and social skills are both important for the development of adolescents' perceived loneliness and that adolescents' familial attachment sets the baseline for neurobiological development. By reviewing the related behavioral and neuroimaging literature, we propose a developmental social neuroscience model to explain the heightened perception of loneliness in adolescents using social skills and attachment style as neurobiological moderators. We encourage future researchers to investigate adolescents' perceived social connectedness from the developmental neuroscience perspective.
60Reduced exosomal miR-215-5p activates the NEAT1/MAPK1/p-CRMP2 pathway and contributes to social dysfunction in a VPA-induced autism model.PubMed
Lian Liu, Liang Xie, Yongchun Shen, et al.
Neuropharmacology. 2025 Nov 1;278:110539. doi: 10.1016/j.neuropharm.2025.110539. Epub 2025 Jun 2.
Autism is a prevalent neurodevelopmental disorder characterized by social deficits. Environmental factors, such as prenatal exposure to valproic acid (VPA), are major risk factors for the development of autism in offspring. Environmental epigenetics investigates how environmental factors influence gene expression and function. Exosomal miRNAs carry epigenetic information, but their role in autism remains unknown. Here, we found that prenatal VPA exposure reduced the majority of exosomal miRNA expressions in male newborn amygdala tissue, with exosomal miR-215-5p showing the highest decline. Reduced exosomal miR-215-5p increased neuronal lncRNA NEAT1 expression. Overexpressed neuronal NEAT1 increased the recruitment of the HSP90AB1-MAPK1-CRMP2 complex, which elevated phosphorylated CRMP2 (p-CRMP2) levels. Enhanced p-CRMP2 acted as an "eat me" signal to microglia, resulting in excessive synaptic pruning and aberrant synaptic maturation. Increasing neuronal p-CRMP2 levels via phosphorylation virus T514E or overexpression of MAPK1 promoted microglial synaptic pruning, leading to synaptic defects and social dysfunction. Furthermore, NEAT1 silencing or MAPK1 inhibition reversed the elevated p-CRMP2 levels in VPA-exposed offspring, hence preventing excessive synaptic pruning and social dysfunction. These findings suggested that prenatal VPA exposure reduced exosomal miR-215-5p and activated NEAT1/MAPK1/p-CRMP2 pathway, which resulted in abnormal synaptic development and social interaction disorders.
61Rapid Progressive Social Development of Zebrafish.PubMed
Sarah J Stednitz, Philip Washbourne
Zebrafish. 2020 Feb;17(1):11-17. doi: 10.1089/zeb.2019.1815. Epub 2020 Jan 13.
Zebrafish () are highly social animals that engage in a diverse variety of nonreproductive social behaviors that emerge as early as 14 days postfertilization (dpf). However, we observe considerable behavioral variability at this stage, and comparisons across studies are potentially complicated both by chronological gaps in measurements and inconsistencies in developmental staging. To address these issues, we adapted our assay for social orienting and cueing in the adult zebrafish and used it to probe behavior in a critical window of larval development. In addition, we performed measurements of body length and tested a cohort of larvae with impaired growth to understand if this morphological feature is predictive of individual sociality. We report that zebrafish exhibit increasingly complex social behaviors between 10 and 16 dpf, including place preference, orienting, and social cueing. Furthermore, social behavior is related to standard length on an individual basis beginning at 14 dpf, such that developmentally stunted 14 dpf zebrafish raised on dry feed do not exhibit social behaviors, suggesting some morphological features are more predictive than chronological age. This highly variable and early stage in development provides an opportunity to further understand how genetic and environmental factors affect the assembly of neural circuits underlying complex behaviors.
62Fenpropathrin causes alterations in locomotion and social behaviors in zebrafish (Danio rerio).PubMed
Sian-Tai Liu, Jiun-Lin Horng, Li-Yih Lin, et al.
Aquat Toxicol. 2023 Dec;265:106756. doi: 10.1016/j.aquatox.2023.106756. Epub 2023 Nov 7.
Fenpropathrin is one of the widely used pyrethroid pesticides in agriculture and is frequently detected in the environment, groundwater, and food. While fenpropathrin was found to have neurotoxic effects in mammals, it remains unclear whether it has similar effects on fish. Here, we used adult zebrafish to investigate the impacts of fenpropathrin on fish social behaviors and neural activity. Exposure of adult zebrafish to 500 ppb of fenpropathrin for 72 h increased anxiety levels but decreased physical fitness, as measured by a novel tank diving test and swimming tunnel test. Fish exposed to fenpropathrin appeared to spend more time in the conspecific zone of the tank, possibly seeking greater comfort from their companions. Although learning, memory, and aggressive behavior did not change, fish exposed to fenpropathrin appeared to have shorter fighting durations. The immunocytochemical results showed the tyrosine hydroxylase antibody-labeled dopaminergic neurons in the teleost posterior tuberculum decreased in the zebrafish brain. According to a quantitative polymerase chain reaction (qPCR) analysis of the brain, exposure to fenpropathrin resulted in a decrease in the messenger (m)RNA expression of monoamine oxidase (mao), an enzyme that facilitates the deamination of dopamine. In contrast, the mRNA expression of the sncga gene, which may trigger Parkinson's disease, was found to have increased. There were no changes observed in expressions of genes related to antioxidants and apoptosis between the control and fenpropathrin-exposed groups. We provide evidence to demonstrate the defect of the neurotoxicity of fenpropathrin toward dopaminergic neurons in adult zebrafish.
63Foraging networks and social tolerance in a cooperatively breeding primate (Callithrix jacchus).PubMed
María Fernanda De la Fuente, Cédric Sueur, Paul A Garber, et al.
J Anim Ecol. 2022 Jan;91(1):138-153. doi: 10.1111/1365-2656.13609. Epub 2021 Oct 31.
Within-group competition over food resources can be a major cost of social living. In the wild, foragers are confronted with social (e.g. hierarchical rank) and ecological (e.g. food availability and distribution) challenges that affect their foraging decisions and feeding success. Exhibiting prosocial behaviours, such as tolerance at feeding sites, can benefit group members by developing affiliative social relationships, enhancing access to resources and maximizing fitness. We examined social tolerance at feeding sites in Callithrix jacchus, a cooperatively breeding primate species. We investigated the set of social (rank, age and sex) and ecological (food availability) factors that influence the structure and dynamics of within-group foraging association networks. We designed and conducted an experimental field study of four wild groups of common marmosets in which we controlled food distribution (concentrated or scattered) and productivity (high, medium or low food rewards). Then, we used social network analyses to assess the number and strength of foraging associations among group members, their effects on individual food consumption, and whether recent experiences with conspecifics during foraging affected subsequent associations. Overall, common marmoset foraging association networks were cohesive, as group members jointly occupied feeding sites. The number and strength of associations varied depending on the ecological context. Associations were stronger during conditions in which food was concentrated at a single site. Individuals obtained greater access to food resources when sharing a feeding site with conspecifics, but once a food item was obtained, the forager moved to a nearby tree and consumed it away from others. Additionally, the strength of previous foraging associations and subsequent levels of social tolerance at feeding sites were positively related, a relationship compatible with the ability of memorizing associations over time and recalling the information in future decision-making. In sum, marmosets adjusted their partner choices and the strength of foraging associations in response to food availability. They exhibited increased social tolerance at feeding sites during conditions in which opportunities for contest competition were expected to be greatest. These cooperative breeding primates appear to mutually benefit by maintaining cohesive and strong affiliative relationships, and by increasing opportunities for coordinated behaviour and offspring survival.
64The adaptive value of density-dependent habitat specialization and social network centrality.PubMed
Quinn M R Webber, Michel P Laforge, Maegwin Bonar, et al.
Nat Commun. 2024 May 24;15(1):4423. doi: 10.1038/s41467-024-48657-8.
Density dependence is a fundamental ecological process. In particular, animal habitat selection and social behavior often affect fitness in a density-dependent manner. The Ideal Free Distribution (IFD) and niche variation hypothesis (NVH) present distinct predictions associated with Optimal Foraging Theory about how the effect of habitat selection on fitness varies with population density. Using caribou (Rangifer tarandus) in Canada as a model system, we test competing hypotheses about how habitat specialization, social behavior, and annual reproductive success (co)vary across a population density gradient. Within a behavioral reaction norm framework, we estimate repeatability, behavioral plasticity, and covariance among social behavior and habitat selection to investigate the adaptive value of sociality and habitat selection. In support of NVH, but not the IFD, we find that at high density habitat specialists had higher annual reproductive success than generalists, but were also less social than generalists, suggesting the possibility that specialists were less social to avoid competition. Our study supports niche variation as a mechanism for density-dependent habitat specialization.
65Stocking density and feed barrier design affect the feeding and social behavior of dairy cattle.PubMed
J M Huzzey, T J DeVries, P Valois, et al.
J Dairy Sci. 2006 Jan;89(1):126-33. doi: 10.3168/jds.S0022-0302(06)72075-6.
The objectives of this study were to: 1) evaluate how stocking density at the feed bunk affects feeding and social behavior of dairy cows; and 2) determine if this effect is further influenced by the type of feed barrier used. Thirty-six lactating Holstein cows, allotted to 4 groups, were subjected to each of 4 stocking density treatments and 2 feed barrier treatments. Initially, 2 groups were assigned to a headlock barrier, and 2 groups to a post-and-rail barrier. Each group was then exposed to 4 stocking density treatments (0.81, 0.61, 0.41, and 0.21 m/cow, corresponding to 1.33, 1.00, 0.67, and 0.33 headlocks/cow), in 4 successive 10-d treatment periods. After these periods, the feed barriers were switched between groups and the 4 stocking density treatments were readministered. Time-lapse video was used to quantify feeding, standing, and aggressive behavior at the feed bunk. Daily feeding times were greater and duration of inactive standing in the feeding area was less when using a post-and-rail compared with a headlock feed barrier. Feeding time decreased and inactive standing increased for both barrier designs as stocking density increased at the feed bunk. Cows were displaced more often from the feeding area when the stocking density was increased, and this effect was greater for cows using the post-and-rail feed barrier. Cows ranked lower in the social hierarchy at the feed bunk were displaced more often when feeding at a post-and-rail barrier, particularly at high stocking densities. Therefore, we recommend avoiding overstocking at the feed bunk to increase feeding activity and reduce competition. Use of a barrier that provides some physical separation between adjacent cows, such as a headlock feed barrier, can be used to further reduce competition at the feed bunk.
66Social dynamics and behavior of zoo-housed red-footed tortoises at different housing densities.PubMed
Shannon L O'Brien, Addie Diaz, Katherine A Cronin
Behav Processes. 2025 Sep;231:105242. doi: 10.1016/j.beproc.2025.105242. Epub 2025 Jul 28.
Within zoos, it is common for animals that are considered solitary to be housed with conspecifics. This may be due to a variety of factors such as spatial constraints within zoos, difficulties associated with transferring animals, breeding goals, and/or other management challenges. However, the welfare implications of housing solitary animals with conspecifics are not well understood. This opportunistic study examined the impact of different housing densities (two versus four individuals) on red-footed tortoise social dynamics and behavior. Agonistic behaviors, primarily mounting, were significantly higher when four tortoises were present. Additionally, the tortoises utilized more of their enclosure when four tortoises were present. Social network analyses revealed that the tortoises had a dominance hierarchy, with high asymmetry and unidirectionality between tortoise dyads. Further, social inactivity decreased when only two tortoises were present. Collectively, the results of this study provide valuable information about the relationship between housing density and behavior in these tortoises, which can inform future study design and management strategies at other institutions that house reptiles socially.
67City lizards are more social.PubMed
Avery L Maune, Tobias Wittenbreder, Duje Lisičić, et al.
Biol Lett. 2025 Sep;21(9):20250326. doi: 10.1098/rsbl.2025.0326. Epub 2025 Sep 24.
Cities are expanding globally, exposing animals to novel ecological conditions that can alter the frequency and nature of their social interactions. Urban habitat features, such as built infrastructure and patchy resource distributions, can constrain movement and promote aggregation, potentially increasing encounters among conspecifics and introducing unique social challenges. Understanding how urbanization affects social behaviour is therefore crucial. However, these effects remain poorly understood, and studies on solitary or non-gregarious species are particularly scarce. Here, we investigate how urbanization influences social behaviour in the common wall lizard (), a territorial species and successful urban dweller. We constructed social networks using proximity-based association data from urban and non-urban lizard populations. Urban lizards had more social connections, stronger associations and were observed in more associations overall. These differences were not explained by variation in population density. We propose that spatial constraints and resource heterogeneity in urban habitats may enhance social tolerance. Our results reveal that urbanization can reshape social behaviour even in less gregarious species and suggest that shifts in social strategies may facilitate persistence in urban landscapes.
68Microbial Reconstitution Reverses Maternal Diet-Induced Social and Synaptic Deficits in Offspring.PubMed
Shelly A Buffington, Gonzalo Viana Di Prisco, Thomas A Auchtung, et al.
Cell. 2016 Jun 16;165(7):1762-1775. doi: 10.1016/j.cell.2016.06.001.
Maternal obesity during pregnancy has been associated with increased risk of neurodevelopmental disorders, including autism spectrum disorder (ASD), in offspring. Here, we report that maternal high-fat diet (MHFD) induces a shift in microbial ecology that negatively impacts offspring social behavior. Social deficits and gut microbiota dysbiosis in MHFD offspring are prevented by co-housing with offspring of mothers on a regular diet (MRD) and transferable to germ-free mice. In addition, social interaction induces synaptic potentiation (LTP) in the ventral tegmental area (VTA) of MRD, but not MHFD offspring. Moreover, MHFD offspring had fewer oxytocin immunoreactive neurons in the hypothalamus. Using metagenomics and precision microbiota reconstitution, we identified a single commensal strain that corrects oxytocin levels, LTP, and social deficits in MHFD offspring. Our findings causally link maternal diet, gut microbial imbalance, VTA plasticity, and behavior and suggest that probiotic treatment may relieve specific behavioral abnormalities associated with neurodevelopmental disorders. VIDEO ABSTRACT.
69Mechanisms Underlying Microbial-Mediated Changes in Social Behavior in Mouse Models of Autism Spectrum Disorder.PubMed
Martina Sgritta, Sean W Dooling, Shelly A Buffington, et al.
Neuron. 2019 Jan 16;101(2):246-259.e6. doi: 10.1016/j.neuron.2018.11.018. Epub 2018 Dec 3.
Currently, there are no medications that effectively treat the core symptoms of Autism Spectrum Disorder (ASD). We recently found that the bacterial species Lactobacillus (L.) reuteri reverses social deficits in maternal high-fat-diet offspring. However, whether the effect of L. reuteri on social behavior is generalizable to other ASD models and its mechanism(s) of action remains unknown. Here, we found that treatment with L. reuteri selectively rescues social deficits in genetic, environmental, and idiopathic ASD models. Interestingly, the effects of L. reuteri on social behavior are not mediated by restoring the composition of the host's gut microbiome, which is altered in all of these ASD models. Instead, L. reuteri acts in a vagus nerve-dependent manner and rescues social interaction-induced synaptic plasticity in the ventral tegmental area of ASD mice, but not in oxytocin receptor-deficient mice. Collectively, treatment with L. reuteri emerges as promising non-invasive microbial-based avenue to combat ASD-related social dysfunction.
70Metagenome-wide association of gut microbiome features for schizophrenia.PubMed
Feng Zhu, Yanmei Ju, Wei Wang, et al.
Nat Commun. 2020 Mar 31;11(1):1612. doi: 10.1038/s41467-020-15457-9.
Evidence is mounting that the gut-brain axis plays an important role in mental diseases fueling mechanistic investigations to provide a basis for future targeted interventions. However, shotgun metagenomic data from treatment-naïve patients are scarce hampering comprehensive analyses of the complex interaction between the gut microbiota and the brain. Here we explore the fecal microbiome based on 90 medication-free schizophrenia patients and 81 controls and identify a microbial species classifier distinguishing patients from controls with an area under the receiver operating characteristic curve (AUC) of 0.896, and replicate the microbiome-based disease classifier in 45 patients and 45 controls (AUC = 0.765). Functional potentials associated with schizophrenia include differences in short-chain fatty acids synthesis, tryptophan metabolism, and synthesis/degradation of neurotransmitters. Transplantation of a schizophrenia-enriched bacterium, Streptococcus vestibularis, appear to induces deficits in social behaviors, and alters neurotransmitter levels in peripheral tissues in recipient mice. Our findings provide new leads for further investigations in cohort studies and animal models.
71High-fiber diet mitigates maternal obesity-induced cognitive and social dysfunction in the offspring via gut-brain axis.PubMed
Xiaoning Liu, Xiang Li, Bing Xia, et al.
Cell Metab. 2021 May 4;33(5):923-938.e6. doi: 10.1016/j.cmet.2021.02.002. Epub 2021 Mar 1.
Maternal obesity has been reported to be related to neurodevelopmental disorders in the offspring. However, the underlying mechanisms and effective interventions remain unclear. This cross-sectional study with 778 children aged 7-14 years in China indicated that maternal obesity is strongly associated with children's lower cognition and sociality. Moreover, it has been demonstrated that maternal obesity in mice disrupted the behavior and gut microbiome in offspring, both of which were restored by a high-fiber diet in either dams or offspring via alleviating synaptic impairments and microglial maturation defects. Co-housing and feces microbiota transplantation experiments revealed a causal relationship between microbiota and behavioral changes. Moreover, treatment with the microbiota-derived short-chain fatty acids also alleviated the behavioral deficits in the offspring of obese dams. Together, our study indicated that the microbiota-metabolites-brain axis may underlie maternal obesity-induced cognitive and social dysfunctions and that high dietary fiber intake could be a promising intervention.
72Dietary Carbohydrates and Insulin Resistance in Adolescents from Marginalized Areas of Chiapas, México.PubMed
Itandehui Castro-Quezada, Elena Flores-Guillén, Pilar E Núñez-Ortega, et al.
Nutrients. 2019 Dec 16;11(12):3066. doi: 10.3390/nu11123066.
Evidence of the role that dietary carbohydrates (total carbohydrates, dietary fiber, total sugars, dietary glycemic index (GI) and glycemic load (GL)) exerts on insulin levels in adolescents is controversial. Thus, the aim of this study was to assess the association between dietary carbohydrates and insulin resistance in adolescents from Chiapas, México. A cross-sectional study was conducted in 217 adolescents. Sociodemographic, anthropometric, dietary and biochemical data were obtained. Total carbohydrates, dietary fiber, total sugars, dietary GI and GL were calculated from 24 h recalls. Two validated cut-off points for the homeostasis model assessment of insulin resistance (HOMA-IR) were used as surrogates of insulin resistance. Fasting insulin levels ≥ 14.38 μU/mL were considered as abnormal. Multivariate logistic regression models were fitted to assess the association between tertiles of dietary carbohydrates and insulin resistance or hyperinsulinemia. In our study, adolescents with the highest dietary fiber intake had lower odds of HOMA-IR > 2.97 (OR = 0.34; 95% CI: 0.13-0.93) when adjusted for sex, age, body fat percentage and saturated fatty acids intake. No significant associations were found for the rest of the carbohydrate variables. In summary, high-fiber diets reduce the probability of insulin resistance in adolescents from marginalized areas of Chiapas, México.
73Piglets Born from Sows Fed High Fibre Diets during Pregnancy Are Less Aggressive Prior to Weaning.PubMed
Thiago Bernardino, Patricia Tatemoto, Beatrice Morrone, et al.
PLoS One. 2016 Dec 1;11(12):e0167363. doi: 10.1371/journal.pone.0167363. eCollection 2016.
Aggressive interactions, and their consequences, are the most important causes of poor welfare in piglets. Aggressive behaviour can be modulated by the prenatal and neonatal environment in several species. Commercially kept pregnant sows are often subjected to food restriction, which can compromise their welfare. Limited information is available on the consequences of sow hunger during pregnancy on welfare outcomes for their piglets. High fibre diets can mitigate the feeling of hunger and, consequently, it may improve welfare and productivity measures. The aim of this study was to assess the consequences of feeding pregnant gilts with high fibre diets (HFD) on agonistic behaviour, as manifested by skin lesions, and indicators of fear in their piglets at weaning. Twenty-two pregnant gilts were fed either HFD, 12.86% of crude fibre, 2.4 kg per day (N = 14), or low fibre diet (LFD), 2.53% of crude fibre, 2.0 kg per day (N = 8). During lactation, both treatments received the same diet, ad libitum. We investigated the impact of HFD on behaviour and performance measures (birth weight, average daily gain, weaning weight, see S3 File) in the offspring. Skin lesions were evaluated before and after weaning in 156 piglets (100 HFD and 56 LFD), and 142 piglets were subjected to an open field test and a novel object test (87 HFD and 55 LFD). We found no treatment effect on the performance measures. Piglets born from gilts that received HFD had fewer skin lesions before weaning (D28) than the offspring of LFD gilts, while no difference was found during days 29 and 30. In the open field and novel object tests, there was no treatment effect on the behaviour of piglets. The improved skin health at weaning in piglets of sows fed HFD suggests less agonistic interactions amongst these littermates than in piglets of sows fed LFD.
74Effect of rhythm on the recovery from intense exercise.PubMed
Michal Eliakim, Ehud Bodner, Yoav Meckel, et al.
J Strength Cond Res. 2013 Apr;27(4):1019-24. doi: 10.1519/JSC.0b013e318260b829.
Motivational music (music that stimulates physical activity) was previously shown to enhance the recovery from intense exercise. The aim of the present study was to isolate the effect of rhythm (presumed to be the most effective factor of motivational music) on the recovery from intense exercise. Ten young adult active men (age: 26.1 ± 1.7 years) performed 6-minute run at peak oxygen consumption speed, at 3 separate visits (random order). At 1 visit, no music was played during the recovery after exercise. In the other visits, participants listened to motivational music that was previously shown to enhance recovery (a Western CD collection of greatest hits of all times converted to dance style, 140 b·min, strong bit, played by portable MP3 device using headphones at a volume of 70 dB) or only to the rhythm beats derived from the same songs. Mean heart rate (HR), rating of perceived exertion (RPE), number of steps (measured by step counter) and blood lactate concentrations were determined at 3, 6, 9, 12, and 15 minutes of the recovery. There was no difference in HR changes during the recovery at all conditions. Compared with the recovery without music, listening to motivational music during recovery was associated with significant greater number of steps, lower absolute lactate levels, and greater mean decrease of RPE. Listening only to rhythm beats, derived from the same music, during the recovery was associated with significant greater number of steps and lower absolute lactate levels compared to recovery without music. Music was significantly more effective than rhythm only in the absolute mean number of steps. The beneficial effect of both music and rhythm was greater toward the end of the recovery period. Results suggest that listening to music during nonstructured recovery can be used by professional athletes to enhance recovery from intense exercise. Rhythm plays a very important role in the effect of music on recovery and can be used to enhance nonstructured recovery when music is unavailable or when cultural barriers and individual music preferences may apply. The optimal music and rhythm selection is yet to be determined.
75Physiological and Performance Effects of Caffeine Gum Consumed During a Simulated Half-Time by Professional Academy Rugby Union Players.PubMed
Mark Russell, Nicholas A Reynolds, Blair T Crewther, et al.
J Strength Cond Res. 2020 Jan;34(1):145-151. doi: 10.1519/JSC.0000000000002185.
Russell, M, Reynolds, NA, Crewther, BT, Cook, CJ, and Kilduff, L. Physiological and performance effects of caffeine gum consumed during a simulated half-time by professional academy rugby union players. J Strength Cond Res 34(1): 145-151, 2020-Despite the prevalence of caffeine (CAF) as an ergogenic aid, few studies have examined the use of caffeinated gums, especially during half-time in team sports. The physiological (blood lactate and salivary hormone concentrations) and performance (repeated sprints and cognitive function) effects of consuming CAF gum during a simulated half-time were examined. Professional academy rugby union players (n = 14) completed this double-blind, randomized, counterbalanced study. After pre-exercise measurements, players chewed a placebo (PLC) gum for 5 minutes before a standardized warm-up and completing repeated sprint testing (RSSA1). Thereafter, during a 15-minute simulated half-time period, players chewed either CAF (400 mg; 4.1 ± 0.5 mg·kg) or PLC gum for 5 minutes before completing a second repeated sprint test (RSSA2). Blood lactate, salivary testosterone and cortisol concentrations, and indices of cognitive function (i.e., reaction time and Stroop test) were measured at baseline, pre-RSSA1, post-RSSA1, pre-RSSA2, and post-RSSA2. Sprint performance was not affected by CAF (p = 0.995) despite slower sprint times after the first sprint of both RSSA tests (all p < 0.002). After half-time, salivary testosterone increased by 70% (+97 ± 58 pg·ml) in CAF vs. PLC (p < 0.001), whereas salivary cortisol remained unchanged (p = 0.307). Cognitive performance was unaffected by time and trial (all p > 0.05). Although performance effects were absent, chewing CAF gum increased the salivary testosterone concentrations of professional rugby union players over a simulated half-time. Practitioners may, therefore, choose to recommend CAF gum between successive exercise bouts because of the increases in salivary testosterone observed; a variable associated with increased motivation and high-intensity exercise performance.
76Interactive effect of food deprivation and agonistic behavior on blood parameters and muscle glycogen in pigs.PubMed
X Fernandez, M C Meunier-Salaun, P Ecolan, et al.
Physiol Behav. 1995 Aug;58(2):337-45. doi: 10.1016/0031-9384(94)00364-b.
Agonistic behavior, neuroendocrine and plasma metabolite changes, and muscle glycogen content were studied in 16 fed and 16 24 h-fasted domestic Large White pigs (100 +/- 5 kg) submitted to dyadic encounters (30 min) in a novel environment. Comparisons were made with corresponding control pigs (eight fed and eight 24 h-fasted animals) kept under resting conditions. At rest, fasting resulted in a significant decrease in plasma insulin, increase in plasma-free fatty acids, and decrease in glycogen content in the predominantly red Semispinalis muscle. Fasted pigs displayed significantly more submissive acts than fed ones. In response to dyadic encounters, fed and fasted pigs showed similar rise in plasma levels of cortisol, catecholamines, and lactate, but stress-induced hyperglycemia was suppressed in food-deprived animals. Fasting enhanced stress-induced glycogen depletion in the predominantly white Longissimus muscle but this effect was significant only in fast-twitch glycolytic fibres (alpha W). In the Semispinalis of fasted pigs, however, dyadic encounters did not induce further glycogen depletion. The present findings suggest that in response to dyadic encounters, fasting-induced changes in glucose metabolism lead to a higher dependence on endogenous energy reserves, i.e., glycogen, in working muscles.
77Mucosal fungi promote gut barrier function and social behavior via Type 17 immunity.PubMed
Irina Leonardi, Iris H Gao, Woan-Yu Lin, et al.
Cell. 2022 Mar 3;185(5):831-846.e14. doi: 10.1016/j.cell.2022.01.017. Epub 2022 Feb 16.
Fungal communities (the mycobiota) are an integral part of the gut microbiota, and the disruption of their integrity contributes to local and gut-distal pathologies. Yet, the mechanisms by which intestinal fungi promote homeostasis remain unclear. We characterized the mycobiota biogeography along the gastrointestinal tract and identified a subset of fungi associated with the intestinal mucosa of mice and humans. Mucosa-associated fungi (MAF) reinforced intestinal epithelial function and protected mice against intestinal injury and bacterial infection. Notably, intestinal colonization with a defined consortium of MAF promoted social behavior in mice. The gut-local effects on barrier function were dependent on IL-22 production by CD4 T helper cells, whereas the effects on social behavior were mediated through IL-17R-dependent signaling in neurons. Thus, the spatial organization of the gut mycobiota is associated with host-protective immunity and epithelial barrier function and might be a driver of the neuroimmune modulation of mouse behavior through complementary Type 17 immune mechanisms.
78Complex cooperative breeders: Using infant care costs to explain variability in callitrichine social and reproductive behavior.PubMed
Samuel L Díaz-Muñoz
Am J Primatol. 2016 Mar;78(3):372-87. doi: 10.1002/ajp.22431. Epub 2015 Jun 25.
The influence of ecology on social behavior and mating strategies is one of the central questions in behavioral ecology and primatology. Callitrichines are New World primates that exhibit high behavioral variability, which is widely acknowledged, but not always systematically researched. Here, I examine the hypothesis that differences in the cost of infant care among genera help explain variation in reproductive traits. I present an integrative approach to generate and evaluate predictions from this hypothesis. I first identify callitrichine traits that vary minimally and traits that are more flexible (e.g., have greater variance or norm of reaction), including the number of males that mate with a breeding female, mechanisms of male reproductive competition, number of natal young retained, and the extent of female reproductive suppression. I outline how these more labile traits should vary along a continuum of infant care costs according to individual reproductive strategies. At one end of the spectrum, I predict that groups with higher infant care costs will show multiple adult males mating and providing infant care, high subordinate female reproductive suppression, few natal individuals delaying dispersal, and increased reproductive output by the dominant female -with opposite predictions under low infant costs. I derive an estimate of the differences in ecological and physiological infant care costs that suggest an order of ascending costs in the wild: Cebuella, Callithrix, Mico, Callimico, Saguinus, and Leontopithecus. I examine the literature on each genus for the most variable traits and evaluate a) where they fall along the continuum of infant care costs according to their reproductive strategies, and b) whether these costs correspond to the ecophysiological estimates of infant care costs. I conclude that infant care costs can provide a unifying explanation for the most variable reproductive traits among callitrichine genera. The approach presented can be used to generate predictions and motivate researchers to unravel complexity in callitrichine social and reproductive behavior.
80Fitness consequences of outgroup conflict.PubMed
Ines Braga Goncalves, Amy Morris-Drake, Patrick Kennedy, et al.
Elife. 2022 Jul 14;11:e74550. doi: 10.7554/eLife.74550.
In social species across the animal kingdom, conspecific outsiders threaten the valuable resources of groups and their members. This outgroup conflict is recognised as a powerful selection pressure, but we argue that studies explicitly quantifying the fitness consequences need to be broader in scope: more attention should be paid to delayed, cumulative, and third-party fitness consequences, not just those arising immediately to group members involved in physical contests. In the first part of this review, we begin by documenting how single contests can have survival and reproductive consequences either immediately or with a delay. Then, we step beyond contests to describe fitness consequences that can also result from interactions with cues of rival presence and the general landscape of outgroup threat, and beyond single interactions to describe cumulative effects of territorial pressure and elevated outgroup-induced stress. Using examples from a range of taxa, we discuss which individuals are affected negatively and positively, considering both interaction participants and third-party group members of the same or the next generation. In the second part of the review, we provide suggestions about how to move forward. We highlight the importance of considering how different types of outgroup conflict can generate different selection pressures and of investigating variation in fitness consequences within and between species. We finish by discussing the value of theoretical modelling and long-term studies of natural populations, experimental manipulations, and meta-analyses to develop further our understanding of this crucial aspect of sociality.
81Is Oxytocin "Nature's Medicine"?PubMed
C Sue Carter, William M Kenkel, Evan L MacLean, et al.
Pharmacol Rev. 2020 Oct;72(4):829-861. doi: 10.1124/pr.120.019398.
Oxytocin is a pleiotropic, peptide hormone with broad implications for general health, adaptation, development, reproduction, and social behavior. Endogenous oxytocin and stimulation of the oxytocin receptor support patterns of growth, resilience, and healing. Oxytocin can function as a stress-coping molecule, an anti-inflammatory, and an antioxidant, with protective effects especially in the face of adversity or trauma. Oxytocin influences the autonomic nervous system and the immune system. These properties of oxytocin may help explain the benefits of positive social experiences and have drawn attention to this molecule as a possible therapeutic in a host of disorders. However, as detailed here, the unique chemical properties of oxytocin, including active disulfide bonds, and its capacity to shift chemical forms and bind to other molecules make this molecule difficult to work with and to measure. The effects of oxytocin also are context-dependent, sexually dimorphic, and altered by experience. In part, this is because many of the actions of oxytocin rely on its capacity to interact with the more ancient peptide molecule, vasopressin, and the vasopressin receptors. In addition, oxytocin receptor(s) are epigenetically tuned by experience, especially in early life. Stimulation of G-protein-coupled receptors triggers subcellular cascades allowing these neuropeptides to have multiple functions. The adaptive properties of oxytocin make this ancient molecule of special importance to human evolution as well as modern medicine and health; these same characteristics also present challenges to the use of oxytocin-like molecules as drugs that are only now being recognized. SIGNIFICANCE STATEMENT: Oxytocin is an ancient molecule with a major role in mammalian behavior and health. Although oxytocin has the capacity to act as a "natural medicine" protecting against stress and illness, the unique characteristics of the oxytocin molecule and its receptors and its relationship to a related hormone, vasopressin, have created challenges for its use as a therapeutic drug.
82The polyvagal theory: phylogenetic substrates of a social nervous system.PubMed
S W Porges
Int J Psychophysiol. 2001 Oct;42(2):123-46. doi: 10.1016/s0167-8760(01)00162-3.
The evolution of the autonomic nervous system provides an organizing principle to interpret the adaptive significance of physiological responses in promoting social behavior. According to the polyvagal theory, the well-documented phylogenetic shift in neural regulation of the autonomic nervous system passes through three global stages, each with an associated behavioral strategy. The first stage is characterized by a primitive unmyelinated visceral vagus that fosters digestion and responds to threat by depressing metabolic activity. Behaviorally, the first stage is associated with immobilization behaviors. The second stage is characterized by the sympathetic nervous system that is capable of increasing metabolic output and inhibiting the visceral vagus to foster mobilization behaviors necessary for 'fight or flight'. The third stage, unique to mammals, is characterized by a myelinated vagus that can rapidly regulate cardiac output to foster engagement and disengagement with the environment. The mammalian vagus is neuroanatomically linked to the cranial nerves that regulate social engagement via facial expression and vocalization. As the autonomic nervous system changed through the process of evolution, so did the interplay between the autonomic nervous system and the other physiological systems that respond to stress, including the cortex, the hypothalamic-pituitary-adrenal axis, the neuropeptides of oxytocin and vasopressin, and the immune system. From this phylogenetic orientation, the polyvagal theory proposes a biological basis for social behavior and an intervention strategy to enhance positive social behavior.
83The covariation of acoustic features of infant cries and autonomic state.PubMed
Adam Michael Stewart, Gregory F Lewis, Keri J Heilman, et al.
Physiol Behav. 2013 Aug 15;120:203-10. doi: 10.1016/j.physbeh.2013.07.003. Epub 2013 Jul 31.
The evolution of the autonomic nervous system provides an organizing principle to interpret the adaptive significance of physiological systems in promoting social behavior and responding to social challenges. This phylogenetic shift in neural regulation of the autonomic nervous system in mammals has produced a neuroanatomically integrated social engagement system, including neural mechanisms that regulate both cardiac vagal tone and muscles involved in vocalization. Mammalian vocalizations are part of a conspecific social communication system, with several mammalian species modulating acoustic features of vocalizations to signal affective state. Prosody, defined by variations in rhythm and pitch, is a feature of mammalian vocalizations that communicate emotion and affective state. While the covariation between physiological state and the acoustic frequencies of vocalizations is neurophysiologically based, few studies have investigated the covariation between vocal prosody and autonomic state. In response to this paucity of scientific evidence, the current study explored the utility of vocal prosody as a sensitive index of autonomic activity in human infants during the Still Face challenge. Overall, significant correlations were observed between several acoustic features of the infant vocalizations and autonomic state, demonstrating an association between shorter heart period and reductions in heart period and respiratory sinus arrhythmia following the challenge with the dampening of the modulation of acoustic features (fundamental frequency, variance, 50% bandwidth, and duration) that are perceived as prosody.
84Mixed company: a framework for understanding the composition and organization of mixed-species animal groups.PubMed
Eben Goodale, Hari Sridhar, Kathryn E Sieving, et al.
Biol Rev Camb Philos Soc. 2020 Aug;95(4):889-910. doi: 10.1111/brv.12591. Epub 2020 Feb 25.
Mixed-species animal groups (MSGs) are widely acknowledged to increase predator avoidance and foraging efficiency, among other benefits, and thereby increase participants' fitness. Diversity in MSG composition ranges from two to 70 species of very similar or completely different phenotypes. Yet consistency in organization is also observable in that one or a few species usually have disproportionate importance for MSG formation and/or maintenance. We propose a two-dimensional framework for understanding this diversity and consistency, concentrating on the types of interactions possible between two individuals, usually of different species. One axis represents the similarity of benefit types traded between the individuals, while the second axis expresses asymmetry in the relative amount of benefits/costs accrued. Considering benefit types, one extreme represents the case of single-species groups wherein all individuals obtain the same supplementary, group-size-related benefits, and the other extreme comprises associations of very different, but complementary species (e.g. one partner creates access to food while the other provides vigilance). The relevance of social information and the matching of activities (e.g. speed of movement) are highest for relationships on the supplementary side of this axis, but so is competition; relationships between species will occur at points along this gradient where the benefits outweigh the costs. Considering benefit amounts given or received, extreme asymmetry occurs when one species is exclusively a benefit provider and the other a benefit user. Within this parameter space, some MSG systems are constrained to one kind of interaction, such as shoals of fish of similar species or leader-follower interactions in fish and other taxa. Other MSGs, such as terrestrial bird flocks, can simultaneously include a variety of supplementary and complementary interactions. We review the benefits that species obtain across the diversity of MSG types, and argue that the degree and nature of asymmetry between benefit providers and users should be measured and not just assumed. We then discuss evolutionary shifts in MSG types, focusing on drivers towards similarity in group composition, and selection on benefit providers to enhance the benefits they can receive from other species. Finally, we conclude by considering how individual and collective behaviour in MSGs may influence both the structure and processes of communities.
85Evidence of age-related improvement in the foraging efficiency of Adélie penguins.PubMed
Amélie Lescroël, Grant Ballard, Melanie Massaro, et al.
Sci Rep. 2019 Mar 4;9(1):3375. doi: 10.1038/s41598-019-39814-x.
Age variation in reproductive performance is well-documented but the mechanisms underlying this variation remain unclear. Foraging efficiency is likely to be a key source of demographic variation as it determines the amount of energy that can be invested in fitness-related activities. Evidence of age-related changes in the foraging efficiency of adult seabirds is scarce and inconsistent. We investigated the effects of age on the foraging efficiency of breeding Adélie penguins, a relatively short-lived seabird species, in order to gain a broader perspective on the processes driving variation in ageing rates. We found support for a positive effect of age, either linear or levelling off at old ages, on both our proxies for daily catch rate and catch per unit effort. Across all age classes, males were more performant foragers than females. We found no strong evidence for differing ageing patterns between sexes or individual quality levels, and no evidence for senescence. We infer that continuous individual improvement could be responsible for a larger amount of the variation in foraging efficiency with age at our study site, compared with selective disappearance of underperforming phenotypes. The different results reported by other studies highlight the need to conduct longitudinal studies across a range of species in different environments.
86Selective attention in peacocks during assessment of rival males.PubMed
Jessica L Yorzinski, Gail L Patricelli, Siarhei Bykau, et al.
J Exp Biol. 2017 Mar 15;220(Pt 6):1146-1153. doi: 10.1242/jeb.150946.
Males in many species compete intensely for access to females. In order to minimize costly interactions, they can assess their rivals' competitive abilities by evaluating traits and behaviors. We know little about how males selectively direct their attention to make these assessments. Using Indian peafowl () as a model system, we examined how males visually assess their competitors by continuously tracking the gaze of freely moving peacocks during the mating season. When assessing rivals, peacocks selectively gazed toward the lower display regions of their rivals, including the lower eyespot and fishtail feathers, dense feathers, body and wings. Their attention was modified based on the rivals' behavior such that they spent more time looking at rivals when rivals were shaking their wings and moving. The results indicate that peacocks selectively allocate their attention during rival assessment. The gaze patterns of males assessing rivals were largely similar to those of females evaluating mates, suggesting that some male traits serve a dual function in both intra- and intersexual selection. However, males spent more time than females looking at the upper eyespots and this could indicate that the upper eyespots function more in close-up rival assessment than mate choice.
87When less is more: coy display behaviours and the temporal dynamics of animal courtship.PubMed
Thomas MacGillavry, Giovanni Spezie, Leonida Fusani
Proc Biol Sci. 2023 Oct 11;290(2008):20231684. doi: 10.1098/rspb.2023.1684. Epub 2023 Oct 4.
Sexual selection research has been dominated by the notion that mate choice selects for the most vigorous displays that best reflect the quality of the courter. However, courtship displays are often temporally structured, containing different elements with varying degrees of intensity and conspicuousness. For example, highly intense movements are often coupled with more subtle components such as static postures or hiding displays. Here, we refer to such subtle display traits as 'coy', as they involve the withholding of information about maximal display capabilities. We examine the role of intensity variation within temporally dynamic displays, and discuss three hypotheses for the evolution of coy courtship behaviours. We first review the threat reduction hypothesis, which points to sexual coercion and sexual autonomy as important facets of sexual selection. We then suggest that variation in display magnitude exploits pre-existing perceptual biases for temporal contrast. Lastly, we propose that information withholding may leverage receivers' predispositions for filling gaps in information-the 'curiosity bias'. Overall, our goal is to draw attention to temporal variation in display magnitude, and to advocate possible scenarios for the evolution of courtship traits that regularly occur below performance maxima. Throughout, we highlight novel directions for empirical and theoretical investigations.
88Neural and molecular mechanisms underlying female mate choice decisions in vertebrates.PubMed
Ross S DeAngelis, Hans A Hofmann
J Exp Biol. 2020 Sep 6;223(Pt 17):jeb207324. doi: 10.1242/jeb.207324.
Female mate choice is a dynamic process that allows individuals to selectively mate with those of the opposite sex that display a preferred set of traits. Because in many species males compete with each other for fertilization opportunities, female mate choice can be a powerful agent of sexual selection, often resulting in highly conspicuous traits in males. Although the evolutionary causes and consequences of the ornamentation and behaviors displayed by males to attract mates have been well studied, embarrassingly little is known about the proximate neural mechanisms through which female choice occurs. In vertebrates, female mate choice is inherently a social behavior, and although much remains to be discovered about this process, recent evidence suggests the neural substrates and circuits underlying other fundamental social behaviors (such as pair bonding, aggression and parental care) are likely similarly recruited during mate choice. Notably, female mate choice is not static, as social and ecological environments can shape the brain and, consequently, behavior in specific ways. In this Review, we discuss how social and/or ecological influences mediate female choice and how this occurs within the brain. We then discuss our current understanding of the neural substrates underlying female mate choice, with a specific focus on those that also play a role in regulating other social behaviors. Finally, we propose several promising avenues for future research by highlighting novel model systems and new methodological approaches, which together will transform our understanding of the causes and consequences of female mate choice.
89Recent advances in noninvasive techniques to monitor hormone-behavior interactions.PubMed
P L Whitten, D K Brockman, R C Stavisky
Am J Phys Anthropol. 1998;Suppl 27:1-23. doi: 10.1002/(sici)1096-8644(1998)107:27+<1::aid-ajpa2>3.0.co;2-h.
This paper reviews recent advances in field endocrinology, a focus as well as a method in primatology and behavioral ecology that permits the examination of social behavior and life history through hormonal investigations in natural settings. Endocrine data complements the traditional behavioral data collected by field scientists by providing quantitative measures for the examination of adaptive tradeoffs, costs of social strategies, and reproductive and social significance of mating events. Further, investigations of the physiological mechanisms of reproductive constraint provide tests of the adaptive significance of reproductive skew in cooperative and competitive breeders. Hormone data also can provide insights into the costs of competition and aggression and the role of temperament in individual reproductive success and the evolution of social systems. New, noninvasive methods for the collection of this information have augmented and expanded field endocrinology through the use of techniques that do not require potentially confounding physical or physiological manipulations. Specifically, urine and fecal samples can be collected from free-ranging animals and contain gonadal and adrenal hormones that parallel profiles of serum hormones. Sampling, preservation, extraction, and assay methods for the analysis of excreted steroids are reviewed along with the species and questions to which these methods have been applied.
90Fluctuating selection strength and intense male competition underlie variation and exaggeration of a water strider's male weapon.PubMed
William Toubiana, Abderrahman Khila
Proc Biol Sci. 2019 Apr 24;286(1901):20182400. doi: 10.1098/rspb.2018.2400.
Sexually selected traits can reach high degrees of phenotypic expression and variation under directional selection. A growing number of studies suggest that such selection can vary in space, time and form within and between populations. However, the impact of these fluctuations on sexual trait evolution is poorly understood. In the water strider Microvelia longipes, males display striking trait exaggeration and phenotypic variation manifested as extreme differences in the rear leg length. To study the origin and maintenance of this exaggerated trait, we conducted comparative behavioural, morphometric and reaction norm experiments in a selection of Microvelia species. We uncovered differences both in the mating behaviour and the degree of sexual dimorphism across these species. Interestingly, M. longipes evolved a specific mating behaviour where males compete for egg-laying sites, consisting of small floating objects, to intercept and copulate with gravid females. Through male-male competition assays, we demonstrated that male rear legs are used as weapons to dominate egg-laying sites and that intense competition is associated with the evolution of rear leg length exaggeration. Field observations revealed rapid fluctuation in M. longipes habitat stability and the abundance of egg-laying sites. Paternity tests using genetic markers demonstrated that small males could only fertilize about 5% of the eggs when egg-laying sites are limiting, whereas this proportion increased to about 20% when egg-laying sites become abundant. Furthermore, diet manipulation and artificial selection experiments also showed that the exaggerated leg length in M. longipes males is influenced by both genetic and nutritional factors. Collectively, our results highlight how fluctuation in the strength of directional sexual selection, through changes in the intensity of male competition, can drive the exaggeration and phenotypic variation in this weapon trait.
91Human cooperation and evolutionary transitions in individuality.PubMed
Cathryn Townsend, Joseph V Ferraro, Heather Habecker, et al.
Philos Trans R Soc Lond B Biol Sci. 2023 Mar 13;378(1872):20210414. doi: 10.1098/rstb.2021.0414. Epub 2023 Jan 23.
A major evolutionary transition in individuality involves the formation of a cooperative group and the transformation of that group into an evolutionary entity. Human cooperation shares principles with those of multicellular organisms that have undergone transitions in individuality: division of labour, communication, and fitness interdependence. After the split from the last common ancestor of hominoids, early hominins adapted to an increasingly terrestrial niche for several million years. We posit that new challenges in this niche set in motion a positive feedback loop in selection pressure for cooperation that ratcheted coevolutionary changes in sociality, communication, brains, cognition, kin relations and technology, eventually resulting in egalitarian societies with suppressed competition and rapid cumulative culture. The increasing pace of information innovation and transmission became a key aspect of the evolutionary niche that enabled humans to become formidable cooperators with explosive population growth, the ability to cooperate and compete in groups of millions, and emergent social norms, e.g. private property. Despite considerable fitness interdependence, the rise of private property, in concert with population explosion and socioeconomic inequality, subverts potential transition of human groups into evolutionary entities due to resurgence of latent competition and conflict. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.