1. 分类学定位：白蚁属于蟑螂的系统发育证据
1.1 昆虫分类学框架下的Blattodea目界定
传统昆虫分类学中，白蚁（Termitoidae，亦称Isoptera）和蟑螂（cockroaches）通常被视为独立的目。然而，随着分子系统学研究的深入，这一分类体系已被修订。现代昆虫分类学框架将白蚁和蟑螂共同归入Blattodea目，明确指出白蚁是蟑螂类群中演化出的一个真社会性分支123。这种修订是基于形态学和分子生物学证据的整合，颠覆了以往的认知，揭示了白蚁与蟑螂之间远比想象中更为紧密的亲缘关系。
具体来说，Blattodea目现在涵盖了所有蟑螂以及白蚁，反映了它们共同的演化起源。白蚁被认为是高度特化的蟑螂类群，是昆虫界中少数几个演化出真社会性（eusociality）的谱系之一4。分子系统发育学研究，特别是基于基因组和转录组数据的分析，强有力地支持了白蚁嵌套于蟑螂内部的分类地位，例如，有研究通过比较美洲大蠊（Periplaneta americana）与两种白蚁的基因序列，发现了高度的同源性，进一步证实了它们的亲缘关系2。这些证据共同描绘了从亚社会性蟑螂向真社会性白蚁的演化路径，为理解两者习性差异的生物学基础奠定了分类学基础。
1.2 分子与形态学的关键证据
白蚁与蟑螂的近缘关系已通过多方面的分子和形态学证据得到确凿证实。在分子层面，对线粒体基因组、核基因以及全基因组数据的分析构建的系统发育树，清晰地将白蚁置于蟑螂目（Blattodea）内，而非其独立的目。例如，一项利用66个线粒体基因组进行的系统发育分析表明，白蚁与隐尾蠊属（Cryptocercus）蟑螂的谱系在大约1.7亿年前（95%置信区间为1.53-1.96亿年前）分化 5。这种时间上的关联，为理解白蚁起源于蟑螂提供了重要的时间尺度。进一步的研究也证实，隐尾蠊属物种的肠道共生体与白蚁的肠道共生体存在相似之处，尤其是一些特定的纤毛虫谱系，如_Oxynympha loricata_，在白蚁和木食性蟑螂中均有发现，这暗示了共同的祖先起源和共生关系 6。
除了基因组学数据，形态学证据也为白蚁与特定蟑螂类群（尤其是木蟑螂，如隐尾蠨属_Cryptocercus_）的亲缘关系提供了支持。隐尾蠊属蟑螂生活在腐烂的木材中，表现出亚社会性行为，如亲代抚育，且其幼虫和成虫依赖肠道共生菌消化木材，这与白蚁的生活习性高度相似 7。更值得注意的是，白蚁和木蟑螂在防御行为上也表现出同源性特征。例如，它们都能通过身体振动产生警报信号，这被认为是二者共享的原始防御机制，而非独立演化出的特征。这种振动警报信号的同源性进一步强化了白蚁源自木蟑螂祖先的观点。尽管白蚁在演化过程中形成了复杂的真社会性结构和多型性个体（如兵蚁），但其与木蟑螂在分子遗传和某些基础生物学特征上的相似性，为我们理解白蚁的演化起源提供了坚实的基础。
2. 社会行为的起源：从亚社会性蟑螂到真社会性白蚁的进化路径
2.1 蟑螂的亚社会性基础
白蚁真社会性的演化并非凭空出现，而是建立在特定蟑螂类群所展现的亚社会性行为之上。隐尾蠊属（Cryptocercus）作为白蚁的姐妹群，是理解这一演化路径的关键模型。这类木食性蟑螂展现出显著的亚社会性特征，被认为是白蚁真社会性起源的“垫脚石”8。
_Cryptocercus_属蟑螂的亚社会性主要体现在以下几个方面：
- 亲代抚育（Parental Care）：_Cryptocercus_物种以单配偶制的形式生活在木质隧道中，亲代会照料它们的后代。例如，韩国隐尾蠊（Cryptocercus kyebangensis）的田间调查显示，有亲代（单亲或双亲）与后代共同生活的家庭最为常见，平均每个家庭的幼虫数量约为21.6只9。亲代抚育是许多亚社会性昆虫的共同特征，并且在从个体生活向社会性演化过程中扮演着重要角色，它涉及亲代对后代的资源投入和行为照护10。
- 共同生活与延长发育周期：隐尾蠊的卵鞘在6月中旬至7月下旬被观察到，并且在亲代与幼虫共同生活的隧道中，卵鞘孵化出的幼虫（若虫）会在冬季到来前生长到三龄或四龄9。这意味着幼虫有一个延长的发育期，且在此期间与亲代共同生活。这种延长发育期为亲代与后代之间建立更紧密的社会互动提供了机会。
- 对木质食物的依赖与共生微生物的传递：隐尾蠊主要以腐木为食，这是一种营养价值较低的食物来源。它们与白蚁一样，肠道内含有帮助消化纤维素的共生微生物。为了确保幼虫能够获得这些必需的共生体，亲代会通过直肠喂养（proctodeal feeding）的方式将共生微生物传递给后代，这种行为在实验室观察中得到了证实9。这种垂直传递的机制是维持其木食性生活方式的关键，也是建立亲代与后代间紧密联系的重要驱动力。
- 未成熟发育（Altricial Development）：与许多其他蟑螂不同，隐尾蠊的初孵幼虫表现出“未成熟发育”的特征，即它们的身体结构相对不完整，如浅色透明的体壁和相对不发达的眼睛11。这种未成熟状态意味着初孵幼虫对亲代抚育的依赖性更强，无法独立生存，必须依赖亲代提供照料和保护。这种高度依赖性被认为是白蚁表型可塑性演化的基础，为后来的群体成员（如工蚁）的个体发育停滞提供了演化模板12。
总而言之，_Cryptocercus_属蟑螂所展现的亲代抚育、共同生活、共生微生物传递以及幼虫的未成熟发育等亚社会性特征，为白蚁真社会性的起源奠定了行为和生理基础。这些特征使得亲代与后代能够长时间共同生活，形成一个相对稳定的家庭单位，从而为后续的劳动分工和多型性个体演化提供了进化的温床。
2.2 真社会性的关键创新：内分泌与基因组调控
白蚁从亚社会性蟑螂祖先演化为真社会性昆虫，其核心创新在于对个体发育可塑性的内分泌和基因组调控，特别是通过保幼激素（Juvenile Hormone, JH）及其相关信号通路实现的高度精细的品级（caste）分化。品级分化是白蚁真社会性的基石，它使得群体内不同个体承担特定功能，从而实现劳动分工。
保幼激素（JH）在品级分化中的核心作用：
JH是昆虫发育和繁殖中的关键激素，它在白蚁的品级分化中发挥着核心的调控作用。研究表明，JH水平的波动是决定白蚁幼体（若虫）向不同品级（如工蚁、兵蚁、补充生殖蚁等）分化的关键因素1314。
- 兵蚁分化：通常，高水平的JH会导致若虫分化为兵蚁。在白蚁群体中，通过人工施用JH类似物（JHA）可以诱导若虫分化为兵蚁前体（presoldier），这一过程与自然条件下JH水平升高密切相关1415。在潮湿木白蚁（Hodotermopsis sjostedti）中，兵蚁分化前会出现JH水平的显著升高14。
- 补充生殖蚁分化：当原始的蚁王蚁后死亡或衰老时，群体会分化出补充生殖蚁来取代它们。研究发现，补充生殖蚁的产生与JH水平降低相关。例如，在_Hodotermopsis sjostedti_中，补充生殖蚁分化过程中JH水平会暂时降低，但在蜕皮前又会升高，显示出JH在协调蜕皮与品级分化中的复杂作用16。补充生殖蚁表现出幼体特征，如无翅，这表明它们的性成熟是在保留幼体形态的情况下发生的，这一过程受JH和蜕皮激素（ecdysone）异时性作用的调控16。
- 与其他品级的关系：工蚁和若虫的JH水平相对较低，促使它们进行非生殖性活动。生殖蚁（蚁王蚁后）在性成熟后，JH水平会升高，以维持生殖功能14。
蟑螂与白蚁的MEKRE93通路对比：
在蟑螂中，JH信号通路，特别是涉及Met、Kr-h1、E93转录因子的MEKRE93通路，调控若虫向成虫的形态转变13。E93基因被认为是“成虫决定基因”，其表达水平决定了昆虫是否蜕变为成虫。
- 蟑螂中的MEKRE93通路：在蟑螂中，低JH水平会促进E93的表达，从而诱导昆虫蜕变为成虫13。
- 白蚁中的MEKRE93通路与社会性适应：在白蚁中，该通路被“征用”并适应性演化，以调控品级分化而非简单的若虫-成虫转变。研究推测，白蚁的品级可能通过JH在MEKRE93通路中的调制作用而确定13。例如，在白蚁兵蚁分化过程中，JH与蜕皮激素（20E）信号传导之间的调节机制，可能涉及TGFβ信号相关基因的参与，这些基因可能被征用，以在JH和20E信号之间进行调节，从而促成兵蚁的特化发育17。对蟑螂和白蚁的关键品级调控基因（如Met，JH受体）进行比较研究发现，JH-Met信号在两者中都与蜕皮激活相关，但JH受体与20E信号之间的调控机制在白蚁兵蚁形态发生中是特异性的18。这表明在白蚁的社会性演化中，原有的激素信号通路发生了功能上的重编程。
基因组研究中的放松选择与基因适应性进化：
白蚁的真社会性演化伴随着基因组层面的显著变化，包括基因重复和适应性进化1920。
- 基因重复与品级相关基因扩张：基因重复在白蚁的社会性演化中扮演了重要角色，使得特定基因家族得以扩张，并产生新的功能或亚功能化，从而促进了品级特异性功能的出现1920。例如，白蚁基因组中与社会功能相关的各类基因（如脂运载蛋白、纤维素酶、溶菌酶、香叶基香叶基二磷酸合酶）出现了显著重复，这些重复基因的表达模式往往表现出品级偏向性19。这些基因的重复和随后的分化，使得白蚁能够发展出复杂的社会行为和生理功能，例如复杂的化学通讯、高效的木材消化能力、强大的社会免疫以及专门的防御机制19。
- 生殖和发育相关基因的适应性进化：白蚁群体内部的生殖分工（仅有少数个体负责生殖）可能导致生殖相关基因受到放松选择，从而使这些基因在非生殖品级中积累突变，并可能被重新利用于其他功能，从而促进了品级多样化。例如，生殖和发育相关基因的重复被认为是白蚁真社会性起源的关键因素20。
- 发育途径多样化：不同白蚁类群的品级发育途径存在差异，这可能与特定基因（如_Doublesex_）表达模式的谱系特异性变化有关。_Doublesex_基因在一些白蚁中表现出品级间的表达差异，尤其是在雄性生殖蚁与雄性不育品级之间，这可能反映了品级发育途径多样化的潜在机制20。
综上所述，白蚁真社会性的起源是一个多层次的演化过程，它涉及内分泌系统（特别是JH）对个体发育可塑性的精细调控、原有信号通路（如MEKRE93）的功能重编程，以及基因组层面的适应性变化（如基因重复和功能分化），这些共同促成了白蚁复杂而高效的社会结构的形成。
3. 生理与生态适应的分化：习性差异的功能基础
3.1 食性与共生微生物的特化
白蚁和蟑螂在食性上表现出显著的分化，这深刻影响了它们的肠道微生物群落组成、营养获取策略以及共生关系的演化。白蚁以其独特的木食性而闻名，主要依赖木质纤维素类生物质，而蟑螂则通常是杂食性，食谱更为广泛。这种食性差异是其习性分化的功能基础之一。
白蚁的木食性与共生微生物的特化：
白蚁是高效的木质纤维素降解者，这一能力主要得益于其肠道中高度特化的共生微生物群落。
- 木质纤维素降解能力：白蚁能够消化包括木材在内的多种木质纤维素生物质，即使是木质素含量高的材料也能有效利用 21。这种能力是由其肠道内密集且多样化的微生物群落提供的，这些微生物在共生消化中发挥着至关重要的作用 22。
- 微生物群落组成：低等白蚁主要依赖独特的纤维素降解鞭毛虫，而高等白蚁则仅含有细菌和古细菌 22。这些微生物群落的功能及其在不同食性群体中的分布正在逐步揭示。例如，来自白蚁肠道的宏基因组分析发现，细菌中的拟杆菌门（Bacteroidota）和螺旋体门（Spirochaetota）是低等白蚁中纤维素分解酶的主要来源，它们主要负责降解纤维二糖，而半纤维素降解则更为多样 23。高等白蚁肠道中的微生物则拥有更全面的内切和外切葡聚糖酶，类似于白蚁肠道鞭毛虫的酶系统，这表明在失去鞭毛虫后，某些细菌门类（如厚壁菌门和螺旋体门）占据了纤维素分解的生态位 23。此外，变形菌门（Pseudomonadota）和放线菌门（Actinomycetota）的微生物在后肠壁外围富集，含有氧化纤维素或修饰木质素的酶，揭示了氧气在木质素解聚中未被充分认识的作用 23。
- 垂直传递机制：白蚁的社会行为降低了群落组装的随机性，促进了共进化，并最终可能导致协同物种形成 22。真菌培养白蚁（如Macrotermitinae亚科）与真菌共生体（如Termitomyces属）之间的互惠共生关系，通过垂直传递来维持 24。这意味着新的白蚁群体在建立时，会从亲代群体继承这些关键的共生体 25。这种严格的垂直传递，确保了共生真菌和细菌群落在世代间的高度保守性和高效性。例如，有研究发现，白蚁后代菌群的44%可遗传自亲代菌群，包括80多个细菌属以及谱系特异性菌株 25。蚁王蚁后在共生菌的跨代传递中扮演关键角色，确保了核心的宿主特异性共生菌（主要为螺旋体门）能从亲代群体传递给后代 26。
- 酶活性：白蚁肠道微生物，特别是厚壁菌门细菌，富含糖苷水解酶（GH），这些酶对于植物生物质的降解至关重要，特别是纤维素分解酶 27。这些微生物与白蚁宿主共同作用，优化了木质素和木质纤维素的分解，以获取营养 28。
蟑螂的广泛食性与微生物群落：
与白蚁不同，蟑螂通常具有更广泛的食谱，从腐烂的有机物到人类食物残渣，甚至在特定条件下也会取食木材。
- 杂食性：例如，美洲大蠊（Periplaneta americana）是杂食性昆虫，其后肠微生物群落多样且稳定，即使在饮食发生剧烈长期变化后也能保持稳定 29。德国小蠊（Blattella germanica）的肠道微生物群落则会受到饮食的显著影响，特别是与代谢和消化必需组分相关的细菌 30。
- 微生物群落的塑造因素：蟑螂肠道微生物群落的结构主要受微生境和功能生态位选择力的影响 22。对食腐木蟑螂肠道微生物群落的研究发现，其肠道理化条件与木食性或杂食性蟑螂相似，肠道所有区域均缺氧，pH值呈弱酸性至中性 31。虽然饮食在塑造白蚁肠道微生物群落结构中扮演重要角色，但在食腐木蟑螂中，饮食并非细菌群落结构的主要驱动因素，其肠道微生物群落与杂食性蟑螂高度相似，表明它们实际消化的食物成分在不同食性群体间并无根本差异 31。
- 共生微生物对宿主发育和健康的影响：蟑螂肠道微生物对其宿主的生长和发育至关重要。研究发现，无菌条件下饲养的美洲大蠊幼虫，其消化组织，特别是后中肠和前肠，发育迟缓，表明肠道微生物对组织生长和发育有显著影响 32。这反映了宿主与微生物之间复杂的协同作用，其中宿主依赖微生物辅助复杂多糖的分解和营养供应（如短链脂肪酸） 32。
- 微生物传递方式：蟑螂的微生物群落也表现出系统发育共生现象（phylosymbiosis），即宿主相关微生物群落的相似性与宿主物种的系统发育关系平行 33。虽然白蚁通常通过垂直传递继承大部分关键共生体，但蟑螂，尤其是那些不完全依赖单一营养来源的物种，可能通过环境获取和水平传播来补充其肠道微生物群落 29。在一些真菌培养白蚁中，虽然大部分共生体是垂直传递的，但在某些情况下也观察到水平传递，这表明共生关系可能具有一定的灵活性 34 35。
综上所述，白蚁和蟑螂在食性上的分化导致了其肠道微生物群落的显著差异以及营养获取策略的特化。白蚁高度依赖其共生微生物降解木质纤维素，并发展出高效的垂直传递机制来维持这种共生关系。而蟑螂则展现出更广泛的食性，其肠道微生物群落也更具弹性，能够适应不同的饮食结构，并在一定程度上依赖环境获取和水平传播。这种分化反映了它们在不同生态位中长期适应的结果。
3.2 防御机制的独立演化
白蚁和蟑螂在防御机制上展现出显著的独立演化路径，尽管它们共享某些祖先特征，但为了适应各自的生态位和生活方式，特别是白蚁发展出的真社会性，它们的防御策略发生了深刻的分化。
振动警报信号：同源性与分化
振动警报信号被认为是白蚁与木蟑螂（如_Cryptocercus_）之间的一种行为共近裔性状（ethological synapomorphy），意味着这种信号在它们的共同祖先中就已经存在 36。
- 木蟑螂与白蚁的同源振动信号：隐尾蠊属蟑螂和白蚁都能够通过身体振动产生警报信号。这种振动通常通过头部敲击基质产生，从而在木质环境中长距离传播 36。例如，干木白蚁（Cryptotermes domesticus）可以通过振动信号评估木材的大小，甚至辨别同种和异种白蚁的振动 3738。当受到干扰时，白蚁兵蚁会通过头部敲击基质产生频率在10-20 Hz的脉冲振动，这些信号在地下隧道中传播速度可达130 m/s，并能有效招募其他兵蚁或促使工蚁撤退 39。
- 社会性背景下的强化：在白蚁群体中，振动信号的功能得到了进一步强化和复杂化。工蚁的振动行为会受到生殖蚁或卵的存在的影响，这可能是一种调节群体社会活动的通讯方式 4041。在更高级的白蚁类群（如Neoisoptera）中，振动警报信号变得最为复杂，常常与化学信号结合使用，形成多模式的通讯系统，这被认为对其生态成功至关重要 36。
化学警报信号：独立演化
与振动信号的同源性不同，化学警报信号在蟑螂和白蚁中是独立演化出来的 36。
- 蟑螂的化学防御：许多蟑螂物种会释放化学物质来威慑捕食者。例如，某些蟑螂通过释放挥发性有机化合物（VOCs）来对抗真菌病原体，这些化合物在不同品级之间存在差异 42。捕食者对带有警告色的猎物（如某些蟑螂的拟态）的规避行为，表明视觉信号在防御中发挥作用 43。
- 白蚁的化学防御：白蚁的化学警报信号至少独立演化了两次 36。兵蚁作为白蚁群体中的特化防御品级，在防御中扮演着核心角色 44。它们通常拥有特化的腺体，能够分泌各种防御性化学物质，如萜烯、脂肪酸和蛋白水解酶，这些物质具有驱避、麻痹甚至杀死入侵者的作用。例如，散白蚁（Coptotermes formosanus）的兵蚁能分泌挥发性有机化合物，这些化合物具有抗真菌活性，有助于维持巢穴的无菌环境 42。这些化学物质的成分和组合在不同白蚁物种和品级之间存在高度特异性，反映了对特定捕食者和病原体的适应性 42。
Neoisoptera类群的复杂信号组合：适应群体生活
Neoisoptera是白蚁中演化程度较高的类群，其防御策略体现了对真社会性群体生活的深刻适应，往往结合了振动和化学信号，形成多模式的复杂通讯系统 36。
- 多模式通讯：这种多模式通讯能提供更丰富、更精确的信息，增强群体对威胁的响应速度和效率。例如，振动信号可以迅速传递警报信息到远距离，而化学信号则可以提供更具体的威胁类型或位置信息，引导兵蚁进行精确防御。在受到攻击时，白蚁工蚁会通过身体摇摆（body-shaking）产生振动信号，吸引兵蚁前往危险区域。兵蚁则会利用头部腺体分泌的化学物质，进一步威慑入侵者并标记威胁源。
- 社会免疫的构成：白蚁的防御机制不仅仅是个体行为，更是群体层面的“社会免疫”系统的一部分 45。除了直接的物理和化学防御外，社会免疫还包括了行为防御（如隔离病原体、清理感染个体）、生理防御（如抗菌物质的分泌）以及环境管理（如巢穴的通风和湿度控制）45。这些防御策略的协同作用，使得白蚁群体能够在微生物丰富和捕食者众多的环境中高效生存。
- 品级特化与防御效率：白蚁的兵蚁是专门用于防御的品级，其形态、生理和行为都高度适应了防御功能 44。兵蚁的存在使得白蚁群体能够比单个个体更有效地应对威胁，通过劳动分工提高防御效率。例如，在蚁王蚁后或卵存在的条件下，工蚁的振动行为会增加，这可能是一种向整个群体传递生殖信息的重要振动通讯 4041。这些精密的防御机制和通讯方式，是白蚁在真社会性演化道路上取得成功的关键因素之一。
总而言之，白蚁和蟑螂在防御机制上的分化，是其长期适应各自生态环境和生活方式的结果。白蚁在继承了祖先振动警报信号的基础上，发展出了高度特化的化学防御和多模式通讯，并通过品级分工和复杂的社会免疫系统，将防御效率提升到新的水平，以适应其独特的真社会性群体生活。
4. 发育与资源分配的差异：群体生存策略的转变
4.1 氮素经济的重构：从个体储存到群体循环
氮元素是所有生物体必需的限制性营养因子，对于木食性昆虫来说，从低氮的木材中获取足够的氮尤其具有挑战性。白蚁与木食性蟑螂（如隐尾蠊属_Cryptocercus_）在氮素经济策略上的根本性转变，是其各自生存策略，特别是白蚁真社会性演化的核心驱动力之一。
木蟑螂的氮素储存策略：表皮氮累积
隐尾蠊属蟑螂采用的是一种“氮素储存型经济”策略。它们在长达数年的幼虫发育过程中，通过逐渐增加体型和表皮密度来累积氮元素 46。
- 个体发育与氮素投资：_Cryptocercus_的个体发育是一个渐进的过程，从孵化时浅色、薄且柔软的角质层，逐渐发展到成虫时深色、厚重且高度硬化的角质层。角质层单位重量的氮含量以及儿茶酚胺（catecholamines，与硬化和黑色素形成相关）的含量，都与这种渐进的变色和硬化过程呈正相关 46。这表明_Cryptocercus_将大量的氮投入到个体表皮的构建和硬化中，以适应个体独立生存和抵御外界威胁的需求。
- 蜕皮损失的氮素：_Cryptocercus_每次蜕皮都会伴随着大量的氮素损失。例如，大约两到三年的_Cryptocercus punctulatus_若虫，其蜕皮中含有高达72.9至82.6微克氮/毫克干重 46。如此高的氮素损失意味着每个个体都需要独立地重新获取和积累氮，这限制了其发育速度，也增加了对环境氮源的依赖。
白蚁的氮素循环策略：低表皮氮与群体互惠
与_Cryptocercus_的个体储存策略形成鲜明对比，白蚁发展出了一种“氮素循环型经济”，其特点是表皮氮含量较低，并通过群体行为（如口饲喂和肛饲喂，即trophallaxis）实现高效的氮素循环和资源共享，以适应低氮环境 46。
- 低表皮氮投资与幼态化：白蚁，尤其是工蚁，在发育过程中保持着幼态化的形态，对角质层的投资极小 46。例如，_Neotermes jouteli_白蚁的蜕皮中仅含有0.19微克氮/毫克干重，远低于_Cryptocercus_的蜕皮氮含量 46。这种低表皮氮的策略显著减少了蜕皮过程中的氮素损失，从而将有限的氮资源更多地用于群体内部循环和维持生命活动。
- 群体互惠（Trophallaxis）：口饲喂和肛饲喂是白蚁群体内部高效分配资源、特别是氮素的关键机制。在散白蚁（Coptotermes gestroi）群体中，蜕皮被认为是可回收的富氮资源（约11%的干重是氮）47。通过口饲喂（proctodeal trophallaxis），工蚁可以将富含氮的蜕皮残骸喂食给蚁王、蚁后、兵蚁甚至幼虫 47。研究发现，标记的蜕皮中的免疫球蛋白G（IgG）可以在除了初龄幼虫（L1）之外的所有品级和生命阶段被检测到，其中蚁后和高龄工蚁（W2+）的标记物浓度显著高于卵和L1 47。这证实了蜕皮中的氮素通过群体互惠在群体内广泛循环，有效地将个体发育过程中的氮素损失转化为群体的共享资源。
- 共生固氮与内共生体：白蚁的氮素经济还受益于其肠道共生体，特别是固氮微生物的贡献。许多白蚁肠道中的微生物能够进行生物固氮，将空气中的氮气转化为可利用的氮化合物，从而补充了从木材中获取的不足 4849。此外，白蚁体内普遍存在的内共生细菌_Blattabacterium cuenoti_也扮演了关键角色，它参与氮循环，为宿主提供氨基酸，尤其是在低氮饮食下 5051。在木食性蟑螂_Cryptocercus punctulatus_和白蚁_Mastotermes darwiniensis_中，_Blattabacterium cuenoti_的基因组显示出氨基酸合成途径的退化，这被认为是由于肠道微生物的高保真传递，使得这些宿主能够获得足够的必需氨基酸，从而允许内共生体的基因组“经济化” 5152。
低氮环境的适应性：群体生存优势
白蚁的氮素循环策略是对低氮木材饮食环境的一种高度适应。通过减少个体在表皮上的氮素投资、最大化蜕皮氮素的回收利用，以及依赖共生微生物的固氮作用，白蚁群体能够更有效地管理和分配有限的氮资源。这种从个体储存到群体循环的转变，不仅促进了白蚁品级分化的发生，使得非生殖品级能够以低氮投入维持生命，也增强了整个群体在资源匮乏环境中的生存能力和竞争力。
综上所述，白蚁和木食性蟑螂在氮素经济策略上的根本差异，反映了它们各自在演化过程中对低氮环境的不同适应途径。白蚁通过降低个体发育成本、强化群体内部的氮素循环以及利用共生微生物的固氮能力，成功地重构了其氮素经济，使其能够高效地利用贫瘠的木材资源，并为真社会性的演化奠定了坚实的生理基础。
4.2 发育可塑性与caste系统的维持
白蚁的品级分化和群体分工的稳定性，核心在于其独特的发育可塑性，这与蟑螂的渐进式发育模式形成了鲜明对比。这种可塑性使得白蚁工蚁能够长时间维持未成熟形态（juvenilized），并在特定社会信号和激素调控下，按需分化为其他品级。
白蚁工蚁的未成熟形态（Juvenilized）与蟑螂的渐进发育差异
在蟑螂中，发育过程是渐进式的，若虫（nymph）经过一系列蜕皮逐渐长大，并最终蜕变为性成熟的成虫。每个龄期的若虫在形态上与成虫相似，且通常能够独立生存。例如，木食性蟑螂（如隐尾蠊属）的若虫虽然依赖亲代传递共生微生物，但其个体形态和功能相对完整，能够进行大部分成年活动。
相比之下，白蚁工蚁表现出明显的“幼态化”特征，即它们在形态上维持着若虫的特征，但功能上却是群体的核心劳动力。这种未成熟状态的维持，意味着白蚁在个体发育上引入了一个可逆的“发育停滞”点，允许其在社会需求下进行品级转变。例如，兵蚁的产生通常涉及两个连续的蜕皮过程（工蚁-前兵蚁-兵蚁），而补充生殖蚁则可能通过单次蜕皮从若虫阶段直接分化而来，但也存在雌性工蚁需要两次蜕皮才能分化为补充生殖蚁的情况，这表明白蚁发育路径的复杂性和灵活性 53。这种独特的发育模式使得白蚁能够根据群体需求灵活调整品级组成，是其真社会性成功的关键。
社会互动对JH水平的调控与品级分化
白蚁的发育可塑性并非简单地由基因程序决定，而是受到复杂的社会互动和内分泌调控网络的共同影响，其中保幼激素（Juvenile Hormone, JH）起着核心作用。
- JH在品级分化中的核心作用：JH是调控昆虫发育和变态的关键激素。在白蚁中，JH水平的动态变化直接决定了若虫向不同品级的可塑性分化 1354。例如，高JH水平通常会诱导工蚁向兵蚁分化 55。对台湾乳白蚁（Coptotermes formosanus）工蚁的研究显示，在蜕皮前6天，其JH III浓度会显著升高至80.5 pg/mg，远高于其他阶段（30-41 pg/mg），这可能与蜕皮和消化道微生物群的清除有关 56。JH不仅通过直接作用于发育程序，还可能通过与蜕皮激素（ecdysteroids）的相互作用来调节品级特异性形态的形成 57。
- 社会互动对JH的调制：白蚁群体内部的社会互动是JH水平及其下游发育通路的关键调节者 1358。
- 兵蚁抑制：群体中已有的兵蚁会释放信息素，抑制其他工蚁向兵蚁分化。这种抑制作用很可能通过影响工蚁体内JH的合成或代谢来实现。例如，在有兵蚁存在的情况下，高JH水平可能会导致“退化发育”（体型减小，发育表观退化），而兵蚁的缺失则会诱导前兵蚁的分化 13。这种反馈机制确保了群体内兵蚁数量维持在适宜水平，避免了资源过度投入到防御品级。
- 生殖蚁抑制与替代生殖蚁分化：蚁王蚁后也会通过信息素抑制其他个体分化为补充生殖蚁。当蚁王蚁后缺失时，这种抑制作用解除，使得工蚁或若虫有机会分化为替代生殖蚁，以维持群体的繁殖功能。在这一过程中，低JH水平与向成虫的渐进式蜕皮相关，而生殖蚁的缺失则会诱导替代生殖蚁的发育 13。补充生殖蚁的产生与JH水平的升高密切相关，例如，在日本散白蚁（Reticulitermes speratus）中，补充生殖蚁的JH水平显著高于若虫和工蚁，且JH信号通路相关基因（如_Met_）在腹部高表达，表明JH在生殖能力激活中的关键作用 59。
- Hexamerin蛋白的作用：在地下白蚁（Reticulitermes flavipes）中，一种被称为Hexamerin的储存蛋白被发现可以结合JH，从而调节其在工蚁体内的有效浓度。Hexamerin的表达和活性受到环境和营养条件的调控，这表明其作为一种“环境响应型开关机制”，在协调JH效能和品级多型性中发挥作用 5560。通过RNAi技术沉默Hexamerin基因，可以显著影响下游15个与形态发生相关的基因表达，表明Hexamerin在JH响应基因网络中的重要作用 60。
- 基因组与微RNA（miRNA）调控：除了JH本身，基因组层面的调控也至关重要。例如，对台湾乳白蚁兵蚁分化机制的研究发现，甲氧普烯（JH类似物）处理可以诱导工蚁向兵蚁转化，并伴随着微RNA（miRNA）的差异表达。这些差异表达的miRNA与品级分化形成了复杂的调控网络，并可能通过影响靶基因（如与核糖体生物发生和昼夜节律相关的基因）来调控兵蚁分化 61。研究还发现，在兵蚁和工蚁中特异性表达的miRNA，其中一些在白蚁和膜翅目社会性昆虫的品级分化中也表现出差异表达，提示这些miRNA可能在社会性昆虫的独立演化中发挥了趋同作用 62。
群体内分工的稳定性
白蚁通过上述内分泌和基因组调控机制，维持了群体内分工的动态平衡和稳定性。这种稳定性体现在：
- 资源优化分配：通过JH对品级分化的精细调控，白蚁群体能够根据环境变化和内部需求，灵活调整各品级的比例，从而优化对有限资源的利用。例如，当群体需要更多防御时，JH水平升高促进兵蚁分化；当群体面临生殖压力时，JH水平变化诱导替代生殖蚁的产生。
- 功能特化与效率提升：幼态化的工蚁作为多能性个体，能根据需求分化为不同品级，实现了高度专业化的劳动分工。兵蚁专注于防御，生殖蚁专注于繁殖，工蚁则承担觅食、筑巢、育幼等任务。这种分工极大地提升了整个群体的生存效率和适应能力。
- 社会调节的反馈回路：社会互动（如信息素）与内分泌系统（如JH）之间形成了一个精密的反馈回路，确保品级比例的自动调节。这种调节机制使得白蚁群体即使在外部环境波动的情况下，也能维持其社会结构的稳定性和功能性。
总之，白蚁的发育可塑性是其真社会性成功的基石。工蚁维持的幼态化特征，使得它们能够在JH及其受社会互动影响的动态调控下，按需分化为不同品级。这种精密的内分泌与社会行为的互作，确保了白蚁群体内部高效而稳定的劳动分工，使其成为地球上最具生态优势的社会性昆虫之一。
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参考文献
1Nutritional symbiosis and ecology of host-gut microbe systems in the Blattodea.PubMed
Benjamin C Jahnes, Zakee L Sabree
Curr Opin Insect Sci. 2020 Jun;39:35-41. doi: 10.1016/j.cois.2020.01.001. Epub 2020 Jan 30.
Cockroaches and termites (Order: Blattodea) have been the subject of substantial research attention for over a century due, in part, to a subset of them having a strong propensity to cohabitate with humans and their structures. Recent research has led to numerous insights into their behavior, physiology, and ecology, as well as their ability to harbor taxonomically diverse microbial communities within their digestive systems, which include taxa that contribute to host growth and development. Further, recent investigations into the physiological and behavioral adaptations that enable recalcitrant polysaccharide digestion and the maintenance of microbial symbionts in cockroaches and termites suggests that symbionts contribute significantly to nutrient provisioning and processing.
2The genomic and functional landscapes of developmental plasticity in the American cockroach.PubMed
Sheng Li, Shiming Zhu, Qiangqiang Jia, et al.
Nat Commun. 2018 Mar 20;9(1):1008. doi: 10.1038/s41467-018-03281-1.
Many cockroach species have adapted to urban environments, and some have been serious pests of public health in the tropics and subtropics. Here, we present the 3.38-Gb genome and a consensus gene set of the American cockroach, Periplaneta americana. We report insights from both genomic and functional investigations into the underlying basis of its adaptation to urban environments and developmental plasticity. In comparison with other insects, expansions of gene families in P. americana exist for most core gene families likely associated with environmental adaptation, such as chemoreception and detoxification. Multiple pathways regulating metamorphic development are well conserved, and RNAi experiments inform on key roles of 20-hydroxyecdysone, juvenile hormone, insulin, and decapentaplegic signals in regulating plasticity. Our analyses reveal a high level of sequence identity in genes between the American cockroach and two termite species, advancing it as a valuable model to study the evolutionary relationships between cockroaches and termites.
3Advances in the understanding of Blattodea evolution: Insights from phylotranscriptomics and spermathecae.PubMed
Jin-Lin Liu, Jia-Wei Zhang, Wei Han, et al.
Mol Phylogenet Evol. 2023 May;182:107753. doi: 10.1016/j.ympev.2023.107753. Epub 2023 Mar 9.
Cockroaches, an ancient and diverse group of insects on earth that originated in the Carboniferous, displays a wide array of morphology or biology diversity. The spermatheca is an organ of the insect reproductive system; the diversity of spermathecae might be the adaption to different mating and sperm storage strategies. Yet a consensus about the phylogenetic relationships among the main lineages of Blattodea and the evolution of spermatheca has not been reached until now. Here we added the transcriptome data of Anaplectidae for the first time and supplemented other family level groups (such as Blaberidae, Corydiidae) to address the pending issues. Our results showed that Blattoidea was recovered as sister to Corydioidea, which was strongly supported by molecular evidence. In Blattoidea, (Lamproblattidae + Anaplectidae) + (Cryptocercidae + Termitoidae) was strongly supported by our molecular data. In Blaberoidea, Pseudophyllodromiidae and Blaberidae were recovered to be monophyletic, while Blattellidae was found to be paraphyletic with respect to Malaccina. Ectobius sylvestris + Malaccina discoidalis formed the sister group to other Blaberoidea; Blattellidae (except Malaccina discoidalis) + Nyctiboridae was found as the sister of Blaberidae. Corydiidae was recovered to be non-monophyletic due to the embedding of Nocticola sp. Our ASR analysis of spermatheca suggested that primary spermathecae were present in the common ancestor, and it transformed at least six times during the evolutionary history of Blattodea. The evolution of spermatheca could be described as a unidirectional trend: the increased size to accommodate more sperm. Furthermore, major splits within the existing genera of cockroaches occurred in the Upper Paleogene to Neogene. Our study provides strong support for the relationship among three superfamilies and offers some new insights into the phylogeny of cockroaches. Meanwhile, this study also provides basic knowledge on the evolution of spermathecae and reproductive patterns.
4Wood-feeding cockroaches as models for termite evolution (Insecta: Dictyoptera): Cryptocercus vs. Parasphaeria boleiriana.PubMed
Klaus-Dieter Klass, Christine Nalepa, Nathan Lo
Mol Phylogenet Evol. 2008 Mar;46(3):809-17. doi: 10.1016/j.ympev.2007.11.028. Epub 2007 Dec 7.
Isoptera are highly specialized cockroaches and are one of the few eusocial insect lineages. Cryptocercus cockroaches have appeared to many as ideal models for inference on the early evolution of termites, due to their possible phylogenetic relationship and several shared key attributes in life history. Recently, Pellens, Grandcolas, and colleagues have proposed the blaberid cockroach Parasphaeria boleiriana to be an alternative model for the early evolution in termites. We compare the usefulness of Cryptocercus and P. boleiriana as models for termite evolution. Cryptocercus and lower Isoptera (1) can both feed on comparatively recalcitrant wood, (2) have an obligate, rich and unique hypermastigid and oxymonadid fauna in the hindgut, (3) transfer these flagellates to the next generation by anal trophallaxis, (4) have social systems that involve long-lasting biparental care, and, finally, (5) are strongly suggested to be sister groups, so that the key attributes (1)-(4) appear to be homologous between the two taxa. On the other hand, P. boleiriana (1) feeds on soft, ephemeral wood sources, (2) shows no trace of the oxymonadid and hypermastigid hindgut fauna unique to Cryptocercus and lower Isoptera, nor does it have any other demonstrated obligate relationship with hindgut flagellates, (3) is likely to lack anal trophallaxis, (4) has only a short period of uniparental brood care, and (5) is phylogenetically remote from the Cryptocercus+Isoptera clade. These facts would argue against any reasonable usage of P. boleiriana as a model for the early evolution of Isoptera or even of the clade Cryptocercus+Isoptera. Cryptocercus thus remains an appropriate model-taxon-by-homology for early termite evolution. As compared to P. boleiriana, some other Blaberidae (such as the Panesthiinae Salganea) appear more useful as model-taxa-by-homoplasy for the early evolution of the Cryptocercus+Isoptera clade, as their brooding behavior is more elaborate than in P. boleiriana.
5The evolutionary history of termites as inferred from 66 mitochondrial genomes.PubMed
Thomas Bourguignon, Nathan Lo, Stephen L Cameron, et al.
Mol Biol Evol. 2015 Feb;32(2):406-21. doi: 10.1093/molbev/msu308. Epub 2014 Nov 10.
Termites have colonized many habitats and are among the most abundant animals in tropical ecosystems, which they modify considerably through their actions. The timing of their rise in abundance and of the dispersal events that gave rise to modern termite lineages is not well understood. To shed light on termite origins and diversification, we sequenced the mitochondrial genome of 48 termite species and combined them with 18 previously sequenced termite mitochondrial genomes for phylogenetic and molecular clock analyses using multiple fossil calibrations. The 66 genomes represent most major clades of termites. Unlike previous phylogenetic studies based on fewer molecular data, our phylogenetic tree is fully resolved for the lower termites. The phylogenetic positions of Macrotermitinae and Apicotermitinae are also resolved as the basal groups in the higher termites, but in the crown termitid groups, including Termitinae + Syntermitinae + Nasutitermitinae + Cubitermitinae, the position of some nodes remains uncertain. Our molecular clock tree indicates that the lineages leading to termites and Cryptocercus roaches diverged 170 Ma (153-196 Ma 95% confidence interval [CI]), that modern Termitidae arose 54 Ma (46-66 Ma 95% CI), and that the crown termitid group arose 40 Ma (35-49 Ma 95% CI). This indicates that the distribution of basal termite clades was influenced by the final stages of the breakup of Pangaea. Our inference of ancestral geographic ranges shows that the Termitidae, which includes more than 75% of extant termite species, most likely originated in Africa or Asia, and acquired their pantropical distribution after a series of dispersal and subsequent diversification events.
6Novel Lineages of Oxymonad Flagellates from the Termite Porotermes adamsoni (Stolotermitidae): the Genera Oxynympha and Termitimonas.PubMed
Renate Radek, Katja Meuser, Samet Altinay, et al.
Protist. 2019 Dec;170(6):125683. doi: 10.1016/j.protis.2019.125683. Epub 2019 Oct 21.
The symbiotic gut flagellates of lower termites form host-specific consortia composed of Parabasalia and Oxymonadida. The analysis of their coevolution with termites is hampered by a lack of information, particularly on the flagellates colonizing the basal host lineages. To date, there are no reports on the presence of oxymonads in termites of the family Stolotermitidae. We discovered three novel, deep-branching lineages of oxymonads in a member of this family, the damp-wood termite Porotermes adamsoni. One tiny species (6-10μm), Termitimonas travisi, morphologically resembles members of the genus Monocercomonoides, but its SSU rRNA genes are highly dissimilar to recently published sequences of Polymastigidae from cockroaches and vertebrates. A second small species (9-13μm), Oxynympha loricata, has a slight phylogenetic affinity to members of the Saccinobaculidae, which are found exclusively in wood-feeding cockroaches of the genus Cryptocercus, the closest relatives of termites, but shows a combination of morphological features that is unprecedented in any oxymonad family. The third, very rare species is larger and possesses a contractile axostyle; it represents a phylogenetic sister group to the Oxymonadidae. These findings significantly advance our understanding of the diversity of oxymonads in termite guts and the evolutionary history of symbiotic digestion.
7Biogeography and Phylogeny of Wood-feeding Cockroaches in the Genus Cryptocercus.PubMed
Kiyoto Maekawa, Christine A Nalepa
Insects. 2011 Jul 19;2(3):354-68. doi: 10.3390/insects2030354.
Subsocial, xylophagous cockroaches of the genus Cryptocercus exhibit a disjunct distribution, with representatives in mature montane forests of North America, China, Korea and the Russian Far East. All described species are wingless and dependent on rotting wood for food and shelter at all stages of their life cycle; consequently, their distribution is tied to that of forests and strongly influenced by palaeogeographical events. Asian and American lineages form distinct monophyletic groups, comprised of populations with complex geographic substructuring. We review the phylogeny and distribution of Cryptocercus, and discuss splitting events inferred from molecular data.
8Origin of eusociality in termites: was genetic monogamy essential?PubMed
Christine A Nalepa, Nathan Lo, Kiyoto Maekawa
Curr Opin Insect Sci. 2025 Aug;70:101388. doi: 10.1016/j.cois.2025.101388. Epub 2025 May 13.
A prevalent hypothesis is that 'strict genetic monogamy' was a universal prerequisite for the origin of eusociality in Hymenoptera and Isoptera. Termites, however, do not fit easily into this scenario, particularly since the sister group of termites, the wood-feeding cockroach Cryptocercus, was recently found to be socially but not genetically monogamous. Termites likely evolved from large, physically robust, obligately subsocial cockroaches in an ecological setting where nitrogen conservation was prioritized. The shift to eusociality can originate from such a starting point via sequential delegation of brood care and defensive parental duties to young alloparents and soldiers, respectively, facilitated by reallocation of available nitrogenous resources. Each social transition was dependent on the prior state, and the final step, the shift from parental defense to origination of a soldier caste, coevolved with a decrease in parental body size and cuticular investment, thus freeing nitrogen for channeling into parental reproduction and cuticular armoring of soldiers. One consequence of this reallocation of critical reserves, however, was on the mating system: the now smaller, vulnerable alates were subjected to relentless predation pressure during dispersal and colony foundation. Swarming, tandem running, hasty mate choice, and immediate and permanent sequestration can be viewed as countermeasures to this selection pressure, enforcing genetic monogamy. We propose that any genetic monogamy detected in incipient colonies of extant termites may be a consequence, rather than a cause, of the initial transition to eusociality; if so, it is a derived mating system that may be a fitness cost in termite evolution.
9Colony composition, social behavior and some ecological characteristics of the Korean wood-feeding cockroach (Cryptocercus kyebangensis).PubMed
Yung Chul Park, Philippe Grandcolas, Jae Chun Choe
Zoolog Sci. 2002 Oct;19(10):1133-9. doi: 10.2108/zsj.19.1133.
Korean populations of the genus Cryptocercus occur in forested mountains throughout South Korea. They live in monogamous associations in which parents care for their young in complex woody galleries. Single paired adults (23.2%) and one or both parents with their offspring (28.1%) were found most frequently in the field. Among single-parent families adult females (6.7%) were observed more frequently than adult males (1.4%). In families with single or both parents, the mean brood size was 21.6+/-9.4. Oothecae were observed from mid-June to the late July. Oothecae were found in the galleries of only paired adults and never found in families with nymphs. The mean number of eggs per female was 73.7+/-29.8. Most of neonates grew to the third or fourth instar prior to the winter. During the winter, C. kyebangensis in the field remained almost frozen in their galleries, but ones kept in the laboratory continued to grow during winter. Some characteristics of proctodeal feeding behavior are also described based on laboratory observations. We propose that the cold temperate climate, especially of the winter season, is one of the most important causes for the evolution of unusual life history of Cryptocercus including delayed development of nymphs.
10Offspring genetic effects on maternal care.PubMed
Harry G Potter, David G Ashbrook, Reinmar Hager
Front Neuroendocrinol. 2019 Jan;52:195-205. doi: 10.1016/j.yfrne.2018.12.004. Epub 2018 Dec 18.
Parental care is found widely across animal taxa and is manifest in a range of behaviours from basic provisioning in cockroaches to highly complex behaviours seen in mammals. The evolution of parental care is viewed as the outcome of an evolutionary cost/benefit trade-off between investing in current and future offspring, leading to the selection of traits in offspring that influence parental behaviour. Thus, level and quality of parental care are affected by both parental and offspring genetic differences that directly and indirectly influence parental care behaviour. While significant research effort has gone into understanding how parental genomes affect parental, and mostly maternal, behaviour, few studies have investigated how offspring genomes affect parental care. In this review, we bring together recent findings across different fields focussing on the mechanism and genetics of offspring effects on maternal care in mammals.
11Altricial development in subsocial wood-feeding cockroaches.PubMed
Christine A Nalepa, Kiyoto Maekawa, Keisuke Shimada, et al.
Zoolog Sci. 2008 Dec;25(12):1190-8. doi: 10.2108/zsj.25.1190.
Species in the wood-feeding genus Salganea within the cockroach subfamily Panesthiinae (Blaberidae) typically live in biparental families; their first instars suffer high mortality when removed from adults, and in at least one species, adults are known to feed neonates on oral liquids. In the closely related gregarious wood-feeding genus Panesthia , no parental interaction with offspring is known. We compared the external morphology of first instars of these two genera and found that eye development and cuticular pigmentation at hatching are correlated with social structure. First instars of Panesthia have a dark cuticle and well-developed eyes. First instars of Salganea have a pale, transparent cuticle, and eyes significantly smaller than those of Panesthia relative to adult eye size. The body size of the first-instar of Salganea esakii is significantly smaller than that of Panesthia angustipennis spadica , relative to adult body size (24.0 and 27.4% of adult head-capsule width, respectively), but a more general survey suggests that, overall, neonate size may be similar in the two genera. We compared the first instars of these two taxa of Panesthiinae to those in the biparental, wood-feeding cockroach Cryptocercus (Cryptocercidae) and discuss how decreased investment in both integumentary and ocular development in subsocial cockroaches parallels that seen in altricial vertebrates.
12Altricial development in subsocial cockroach ancestors: foundation for the evolution of phenotypic plasticity in termites.PubMed
Christine A Nalepa
Evol Dev. 2010 Jan-Feb;12(1):95-105. doi: 10.1111/j.1525-142X.2009.00394.x.
Basal termites possess two developmental features that eusocial Hymenoptera lack: the majority of colony members are juveniles whose somatic and reproductive development is temporarily or permanently suspended, and individual development is characterized by extreme phenotypic plasticity. An examination of the literature indicates that the basis for these unique ontogenetic characters is not the prolongation of a pronymphal stage into postembryonic development, as recently suggested. Like other hemimetabolous insects, termites have three embryonic cuticles, and the pronymphal (EC3) cuticle is shed during or shortly after hatch. Nonetheless, a different developmental landmark, dorsal closure, occurs later during embryogenesis in termites than it does in their cockroach relatives, clearly indicating ontogenetic repatterning from an ancestral state. An alternate hypothesis for the origin of isopteran phenotypic plasticity becomes apparent if we remain focused on the phylogenetic and social context of termite evolution. Altricial development occurs in both vertebrate and invertebrate taxa, evolves in response to the parental environment, and is displayed by two distantly related, biparental, wood-feeding cockroaches, including Cryptocercus, the sister-group to termites. It is therefore likely the condition was present in subsocial termite ancestors, and played a complex, multidimensional role in the transition to eusociality. Most relevant to current arguments is that a shift in responsibility for the care of altricial dependents, from parents to the first nutritionally independent nymphs in the family (alloparents), resulted in the developmental stasis of alloparents at a relatively young age. Because early instar cockroaches are not metamorphically competent, these young alloparents would have provided a novel developmental template on which selection could act.
13Juvenile hormone and hemimetabolan eusociality: a comparison of cockroaches with termites.PubMed
Judith Korb, Xavier Belles
Curr Opin Insect Sci. 2017 Aug;22:109-116. doi: 10.1016/j.cois.2017.06.002. Epub 2017 Jun 15.
Termites are social Dictyoptera that evolved eusociality independently from social Hymenoptera. They are characterized by unique developmental plasticity that is the basis of caste differentiation and social organization. As developmental plasticity is a result of endocrine regulation, in order to understand the evolution of termite sociality it is helpful to compare the endocrine underpinning of development between termites and cockroaches. Nijhout and Wheeler (1982) proposed that varying JH titers determine caste differentiation in termites. Based on current results, we extend this model by adding the importance of social interactions. High JH titers in the presence of soldiers lead to regressive development (decrease in body size, apparent regression in development), while an absence of soldiers induces (pre-)soldier differentiation. On the opposite side, low JH titers in colonies headed by reproductives result in progressive molts toward adults, while an absence of reproductives induces development of replacement reproductives. In cockroaches, transcription factors involved in JH signaling, including the adult specifier E93 (the co-called MEKRE93 pathway) regulate the morphogenetic transition between the nymph and the adult. In termites, we speculate that castes might be determined by social effects playing a modulatory action of JH in the MEKRE93 pathway.
14Juvenile hormone titers and caste differentiation in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae).PubMed
Richard Cornette, Hiroki Gotoh, Shigeyuki Koshikawa, et al.
J Insect Physiol. 2008 Jun;54(6):922-30. doi: 10.1016/j.jinsphys.2008.04.017. Epub 2008 May 3.
Termites are social insects, presenting morphologically distinct castes, performing specific tasks in the colony. The developmental processes underlying caste differentiation are mainly controlled by juvenile hormone (JH). Although many fragmentary data support this fact, there was no comparative work on JH titers during the caste differentiation processes. In this study, JH titer variation was investigated using a liquid chromatography-mass spectrometry (LC-MS) quantification method in all castes of the Japanese damp-wood termite Hodotermopsis sjostedti, especially focusing on the soldier caste differentiation pathway, which was induced by treatment with a JH analog. Hemolymph JH titers fluctuated between 20 and 720pg/microl. A peak of JH was observed during molting events for the pseudergate stationary molt and presoldier differentiation, but this peak was absent prior to the imaginal molt. Soldier caste differentiation was generally associated with high JH titers and nymph to alate differentiation with low JH titers. However, JH titer rose in females during alate maturation, probably in relation to vitellogenesis. In comparison, JH titer was surprisingly low in neotenics. On the basis of these results in both natural and artificial conditions, the current model for JH action on termite caste differentiation is discussed and re-appraised.
15The making of the defensive caste: Physiology, development, and evolution of the soldier differentiation in termites.PubMed
Toru Miura, Kiyoto Maekawa
Evol Dev. 2020 Nov;22(6):425-437. doi: 10.1111/ede.12335. Epub 2020 Apr 14.
Termites (Blattodea, Termitoidea, or Isoptera) constitute one of the major lineages of eusocial insects. In termite societies, multiple types of functional individuals, that is, castes, perform divisions of labors to coordinate social behaviors. Among other castes, the soldier caste is distinctive since it is sterile and exclusively specialized into defensive behavior with largely modified morphological features. Therefore, many of the previous studies have been focused on soldiers, in terms of ecology, behavior, and evolution as well as developmental and physiological mechanisms. This article overviews the accumulation of studies especially focusing on the developmental and physiological mechanisms underlying the soldier differentiation in termites. Furthermore, the evolutionary trajectories that have led the acquisition of soldier caste and have diversified the soldier characteristics in association with the social evolution are discussed.
16Hormone-related genes heterochronically and modularly regulate neotenic differentiation in termites.PubMed
Kohei Oguchi, Shigeyuki Koshikawa, Toru Miura
Dev Biol. 2022 May;485:70-79. doi: 10.1016/j.ydbio.2022.02.012. Epub 2022 Mar 4.
Caste development in social insects requires the coordination of molting and metamorphosis during postembryonic development. In termites, i.e., hemimetabolous eusocial insects, caste fate is determined during postembryonic development. However, it is not fully understood how the mechanisms of molting/metamorphosis are regulated in the course of differentiation between reproductive and sterile castes. In termites, only reproductives derived from alates are imagos and other sterile castes (including developmentally-terminal soldier caste) are basically juveniles or nymphs. Furthermore, supplementary reproductives that appear when the original queens and kings die or become senescent, exhibit larval features such as winglessness, and are called neotenics. Therefore, the question of whether neotenics are larvae or imagos is still under debate. In this study, by inducing female neotenic differentiation in a damp-wood termite Hodotermopsis sjostedti, morphological investigations together with juvenile hormone (JH) quantification and expression/functional analyses of genes responsible for molting and/or metamorphosis were carried out. JH titer and expression of one of the downstream genes (Kr-h1) were shown to be temporarily lowered, but increased just prior to the molt into neotenics, while consistently lowered in imaginal molt (i.e., alate differentiation). In contrast, ecdysone-related genes (EcR and E93) were upregulated at both neotenic and alate differentiation, suggesting that the heterochronic actions of ecdysone and JH lead the neotenic differentiation. Moreover, expression analyses, supported by reverse genetic experiments, showed that EcR and E93 were specifically upregulated in genital sternites (EcR and E93) and ovaries (E93) and required for the development of imaginal characters. These results suggest that the resultant mosaic phenotype of female neotenics is due to modular responses of different body parts to hormonal actions.
17TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation.PubMed
Yudai Masuoka, Hajime Yaguchi, Kouhei Toga, et al.
PLoS Genet. 2018 Apr 11;14(4):e1007338. doi: 10.1371/journal.pgen.1007338. eCollection 2018 Apr.
A working knowledge of the proximate factors intrinsic to sterile caste differentiation is necessary to understand the evolution of eusocial insects. Genomic and transcriptomic analyses in social hymenopteran insects have resulted in the hypothesis that sterile castes are generated by the novel function of co-opted or recruited universal gene networks found in solitary ancestors. However, transcriptome analysis during caste differentiation has not been tested in termites, and evolutionary processes associated with acquiring the caste are still unknown. Termites possess the soldier caste, which is regarded as the first acquired permanently sterile caste in the taxon. In this study, we performed a comparative transcriptome analysis in termite heads during 3 molting processes, i.e., worker, presoldier and soldier molts, under natural conditions in an incipient colony of the damp-wood termite Zootermopsis nevadensis. Although similar expression patterns were observed during each molting process, more than 50 genes were shown to be highly expressed before the presoldier (intermediate stage of soldier) molt. We then performed RNA interference (RNAi) of the candidate 13 genes, including transcription factors and uncharacterized protein genes, during presoldier differentiation induced by juvenile hormone (JH) analog treatment. Presoldiers induced after RNAi of two genes related to TGFβ (Transforming growth factor beta) signaling were extremely unusual and possessed soldier-like phenotypes. These individuals also displayed aggressive behaviors similar to natural soldiers when confronted with Formica ants as hypothetical enemies. These presoldiers never molted into the next instar, presumably due to the decreased expression levels of the molting hormone (20-hydroxyecdysone; 20E) signaling genes. These results suggest that TGFβ signaling was acquired for the novel function of regulating between JH and 20E signaling during soldier differentiation in termites.
18A Crucial Caste Regulation Gene Detected by Comparing Termites and Sister Group Cockroaches.PubMed
Yudai Masuoka, Kouhei Toga, Christine A Nalepa, et al.
Genetics. 2018 Aug;209(4):1225-1234. doi: 10.1534/genetics.118.301038. Epub 2018 Jun 22.
Sterile castes are a defining criterion of eusociality; investigating their evolutionary origins can critically advance theory. In termites, the soldier caste is regarded as the first acquired permanently sterile caste. Previous studies showed that juvenile hormone (JH) is the primary factor inducing soldier differentiation, and treatment of workers with artificial JH can generate presoldier differentiation. It follows that a shift from a typical hemimetabolous JH response might be required for soldier formation during the course of termite evolution within the cockroach clade. To address this possibility, analysis of the role of JH and its signaling pathway was performed in the termite and compared with the wood roach , a member of the sister group of termites. Treatment with a JH analog (JHA) induced a nymphal molt in RNA interference (RNAi) of JH receptor () was then performed, and it inhibited the presoldier molt in and the nymphal molt in Knockdown of in both species inhibited expression of 20-hydroxyecdysone (20E; the active form of ecdysone) synthesis genes. However, in , several 20E signaling genes were specifically inhibited by RNAi. Consequently, RNAi of these genes were performed in JHA-treated termite individuals. Knockdown of 20E signaling and nuclear receptor gene, (/) resulted in newly molted individuals with normal worker phenotypes. This is the first report of the JH-Met signaling feature in termites and JH-dependent molting activation is shared by both taxa and mediation between JH receptor and 20E signalings for soldier morphogenesis is specific to termites.
19Genomic and transcriptomic analyses of the subterranean termite : Gene duplication facilitates social evolution.PubMed
Shuji Shigenobu, Yoshinobu Hayashi, Dai Watanabe, et al.
Proc Natl Acad Sci U S A. 2022 Jan 18;119(3). doi: 10.1073/pnas.2110361119.
Termites are model social organisms characterized by a polyphenic caste system. Subterranean termites (Rhinotermitidae) are ecologically and economically important species, including acting as destructive pests. Rhinotermitidae occupies an important evolutionary position within the clade representing a transitional taxon between the higher (Termitidae) and lower (other families) termites. Here, we report the genome, transcriptome, and methylome of the Japanese subterranean termite Our analyses highlight the significance of gene duplication in social evolution in this termite. Gene duplication associated with caste-biased gene expression was prevalent in the genome. The duplicated genes comprised diverse categories related to social functions, including lipocalins (chemical communication), cellulases (wood digestion and social interaction), lysozymes (social immunity), geranylgeranyl diphosphate synthase (social defense), and a novel class of termite lineage-specific genes with unknown functions. Paralogous genes were often observed in tandem in the genome, but their expression patterns were highly variable, exhibiting caste biases. Some of the assayed duplicated genes were expressed in caste-specific organs, such as the accessory glands of the queen ovary and the frontal glands of soldier heads. We propose that gene duplication facilitates social evolution through regulatory diversification, leading to caste-biased expression and subfunctionalization and/or neofunctionalization conferring caste-specialized functions.
20Genomic Features Underlying the Origin of Sociality and the Diversification of Caste Systems in Termites.PubMed
Kokuto Fujiwara, Takateru Oka, Ryusei Ashihara, et al.
Mol Biol Evol. 2025 Oct 29;42(11). doi: 10.1093/molbev/msaf284.
Termite colonies consist of distinct castes whose developmental pathways fall into 2 types and vary among lineages. Understanding caste evolution and the diversification of developmental mechanisms is central to termite evolutionary biology. A recent hypothesis suggests that functional diversification via gene duplication contributed to termite eusocial evolution. However, genome-wide analysis is currently limited to a single species, Reticulitermes speratus, preventing comparisons of differences in gene duplication patterns and caste-specific gene expression among representatives of the 2 alternative developmental pathway types. We performed whole-genome sequencing and RNA-seq across castes from the Japanese population of Zootermopsis nevadensis. Duplicated genes exhibited more caste-specific expression than single-copy genes, supporting their role in functional diversification. Comparison with the closest termite relative, the noneusocial woodroach Cryptocercus punctulatus, identified 58 gene groups specifically duplicated in termites. Among the 147 Z. nevadensis genes in these groups, 88 GO biological process terms, including those related to genitalia morphogenesis, were significantly enriched. Moreover, some gene families duplicated in R. speratus and Z. nevadensis included paralogs highly expressed in termite-specific soldiers. Transcriptome comparisons between caste and sex of Z. nevandensis and R. speratus revealed notable differences reflecting their developmental pathways. In particular, Doublesex expression did not differ among castes in Z. nevadensis, but was significantly higher in male reproductives than in male sterile castes in R. speratus. Our findings support the hypothesis that gene duplications, particularly in reproduction and development, contributed to termite eusociality and suggest that lineage-specific changes in Doublesex-related expression may underlie the diversification of caste developmental pathways.
21Uncovering the Potential of Termite Gut Microbiome for Lignocellulose Bioconversion in Anaerobic Batch Bioreactors.PubMed
Lucas Auer, Adèle Lazuka, David Sillam-Dussès, et al.
Front Microbiol. 2017 Dec 22;8:2623. doi: 10.3389/fmicb.2017.02623. eCollection 2017.
Termites are xylophages, being able to digest a wide variety of lignocellulosic biomass including wood with high lignin content. This ability to feed on recalcitrant plant material is the result of complex symbiotic relationships, which involve termite-specific gut microbiomes. Therefore, these represent a potential source of microorganisms for the bioconversion of lignocellulose in bioprocesses targeting the production of carboxylates. In this study, gut microbiomes of four termite species were studied for their capacity to degrade wheat straw and produce carboxylates in controlled bioreactors. All of the gut microbiomes successfully degraded lignocellulose and up to 45% w/w of wheat straw degradation was observed, with the gut-microbiome displaying the highest levels of wheat straw degradation, carboxylate production and enzymatic activity. Comparing the 16S rRNA gene diversity of the initial gut inocula to the bacterial communities in lignocellulose degradation bioreactors revealed important changes in community diversity. In particular, taxa such as Spirochaetes and Fibrobacteres that were highly abundant in the initial gut inocula were replaced by Firmicutes and Proteobacteria at the end of incubation in wheat straw bioreactors. Overall, this study demonstrates that termite-gut microbiomes constitute a reservoir of lignocellulose-degrading bacteria that can be harnessed in artificial conditions for biomass conversion processes that lead to the production of useful molecules.
22The Gut Microbiota of Termites: Digesting the Diversity in the Light of Ecology and Evolution.PubMed
Andreas Brune, Carsten Dietrich
Annu Rev Microbiol. 2015;69:145-66. doi: 10.1146/annurev-micro-092412-155715. Epub 2015 Jul 16.
Termite guts harbor a dense and diverse microbiota that is essential for symbiotic digestion. The major players in lower termites are unique lineages of cellulolytic flagellates, whereas higher termites harbor only bacteria and archaea. The functions of the mostly uncultivated lineages and their distribution in different diet groups are slowly emerging. Patterns in community structure match changes in the biology of different host groups and reflect the availability of microbial habitats provided by flagellates, wood fibers, and the increasing differentiation of the intestinal tract, which also creates new niches for microbial symbionts. Whereas the intestinal communities in the closely related cockroaches seem to be shaped primarily by the selective forces of microhabitat and functional niche, the social behavior of termites reduces the stochastic element of community assembly, which facilitates coevolution and may ultimately result in cospeciation.
23Unveiling lignocellulolytic potential: a genomic exploration of bacterial lineages within the termite gut.PubMed
João Felipe M Salgado, Vincent Hervé, Manuel A G Vera, et al.
Microbiome. 2024 Oct 15;12(1):201. doi: 10.1186/s40168-024-01917-7.
BACKGROUND: The microbial landscape within termite guts varies across termite families. The gut microbiota of lower termites (LT) is dominated by cellulolytic flagellates that sequester wood particles in their digestive vacuoles, whereas in the flagellate-free higher termites (HT), cellulolytic activity has been attributed to fiber-associated bacteria. However, little is known about the role of individual lineages in fiber digestion, particularly in LT. RESULTS: We investigated the lignocellulolytic potential of 2223 metagenome-assembled genomes (MAGs) recovered from the gut metagenomes of 51 termite species. In the flagellate-dependent LT, cellulolytic enzymes are restricted to MAGs of Bacteroidota (Dysgonomonadaceae, Tannerellaceae, Bacteroidaceae, Azobacteroidaceae) and Spirochaetota (Breznakiellaceae) and reflect a specialization on cellodextrins, whereas their hemicellulolytic arsenal features activities on xylans and diverse heteropolymers. By contrast, the MAGs derived from flagellate-free HT possess a comprehensive arsenal of exo- and endoglucanases that resembles that of termite gut flagellates, underlining that Fibrobacterota and Spirochaetota occupy the cellulolytic niche that became vacant after the loss of the flagellates. Furthermore, we detected directly or indirectly oxygen-dependent enzymes that oxidize cellulose or modify lignin in MAGs of Pseudomonadota (Burkholderiales, Pseudomonadales) and Actinomycetota (Actinomycetales, Mycobacteriales), representing lineages located at the hindgut wall. CONCLUSIONS: The results of this study refine our concept of symbiotic digestion of lignocellulose in termite guts, emphasizing the differential roles of specific bacterial lineages in both flagellate-dependent and flagellate-independent breakdown of cellulose and hemicelluloses, as well as a so far unappreciated role of oxygen in the depolymerization of plant fiber and lignin in the microoxic periphery during gut passage in HT. Video Abstract.
24Vertical transmission as the key to the colonization of Madagascar by fungus-growing termites?PubMed
T Nobre, P Eggleton, D K Aanen
Proc Biol Sci. 2010 Feb 7;277(1680):359-65. doi: 10.1098/rspb.2009.1373. Epub 2009 Oct 14.
The mutualism between fungus-growing termites (Macrotermitinae) and their mutualistic fungi (Termitomyces) began in Africa. The fungus-growing termites have secondarily colonized Madagascar and only a subset of the genera found in Africa is found on this isolated island. Successful long-distance colonization may have been severely constrained by the obligate interaction of the termites with fungal symbionts and the need to acquire these symbionts secondarily from the environment for most species (horizontal symbiont transmission). Consistent with this hypothesis, we show that all extant species of fungus-growing termites of Madagascar are the result of a single colonization event of termites belonging to one of the only two groups with vertical symbiont transmission, and we date this event at approximately 13 Mya (Middle/Upper Miocene). Vertical symbiont transmission may therefore have facilitated long-distance dispersal since both partners disperse together. In contrast to their termite hosts, the fungal symbionts have colonized Madagascar multiple times, suggesting that the presence of fungus-growing termites may have facilitated secondary colonizations of the symbiont. Our findings indicate that the absence of the right symbionts in a new environment can prevent long-distance dispersal of symbioses relying on horizontal symbiont acquisition.
25Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite.PubMed
Veronica M Sinotte, Justinn Renelies-Hamilton, Sergio Andreu-Sánchez, et al.
Proc Biol Sci. 2023 Oct 25;290(2009):20231559. doi: 10.1098/rspb.2023.1559. Epub 2023 Oct 18.
Mutualistic coevolution can be mediated by vertical transmission of symbionts between host generations. Termites host complex gut bacterial communities with evolutionary histories indicative of mixed-mode transmission. Here, we document that vertical transmission of gut bacterial strains is congruent across parent to offspring colonies in four pedigrees of the fungus-farming termite . We show that 44% of the offspring colony microbiome, including more than 80 bacterial genera and pedigree-specific strains, are consistently inherited. We go on to demonstrate that this is achieved because colony-founding reproductives are selectively enriched with a set of non-random, environmentally sensitive and termite-specific gut microbes from their colonies of origin. These symbionts transfer to offspring colony workers with high fidelity, after which priority effects appear to influence the composition of the establishing microbiome. Termite reproductives thus secure transmission of complex communities of specific, co-evolved microbes that are critical to their offspring colonies. Extensive yet imperfect inheritance implies that the maturing colony benefits from acquiring environmental microbes to complement combinations of termite, fungus and vertically transmitted microbes; a mode of transmission that is emerging as a prevailing strategy for hosts to assemble complex adaptive microbiomes.
26Evidence from the gut microbiota of swarming alates of a vertical transmission of the bacterial symbionts in Nasutitermes arborum (Termitidae, Nasutitermitinae).PubMed
Michel Diouf, Vincent Hervé, Philippe Mora, et al.
Antonie Van Leeuwenhoek. 2018 Apr;111(4):573-587. doi: 10.1007/s10482-017-0978-4. Epub 2017 Nov 10.
Studies on termite symbiosis have revealed that significant symbiont lineages are maintained across generations. However, most studies have focused only on the worker caste. Little is known about the gut microbiota of reproductives, the most probable vectors for transmitting these lineages to offspring. Using 16S rRNA gene-based Illumina MiSeq sequencing, we compared the gut microbiota of swarming alates of the higher termite Nasutitermes arborum with those of their nestmates from the parental colony. The OTU-based alpha diversity indices showed that the gut microbiota of the alates was at least as diverse as those of non-reproductive adults. It was largely dominated by Spirochaetes mostly of the Treponema I cluster (63.1% of reads), the same dominant taxa found in soldiers and workers of this species and in workers of closely related Nasutitermes species. The termite-specific lineages also included other representative taxa such as several clusters of Bacteroidetes and Fibrobacteres-TG3 group. The microbiota of alates was dominated by a core set of host-specific lineages (87% of reads, 77.6% of OTUs), which were always present across all castes/stages. This first comprehensive survey of the microbiota of the founding reproductives of these xylophagous higher termites shows that the bulk of the host endogenous symbionts, mostly taxa that cannot thrive outside the gut, are brought from the parent colony. The royal pair therefore seems to be a key player in the transmission of symbionts across generations and thereby in host-symbiont codiversification. The high proportion of fiber-degrading lineages in their gut suggests a wood-rich diet unlike the larval stages.
27Biochemical and structural characterization of a family-9 glycoside hydrolase bioprospected from the termite Syntermes wheeleri gut bacteria metagenome.PubMed
Raul Alcântara Teixeira Lima, Aisel Valle Garay, Tayná Diniz Frederico, et al.
Enzyme Microb Technol. 2025 Sep;189:110654. doi: 10.1016/j.enzmictec.2025.110654. Epub 2025 Apr 16.
Glycosyl hydrolases (GH) are enzymes involved in the degradation of plant biomass. They are important for biorefineries that aim at the sustainable utilization of lignocellulosic residues to generate value-added products. The termite Syntermes wheeleri gut microbiota showed an abundance of bacteria from the phylum Firmicutes, a phylum with enzymes capable of breaking down cellulose and degrading lignin, facilitating the use of plant materials as a food source for termites. Using bioinformatics techniques, cellobiohydrolases were searched for in the gut metagenome of the termite Syntermes wheeleri, endemic to the Cerrado. After selecting sequences of the target enzymes, termite gut microbiome metatranscriptome data were used as the criteria to choose the GH9 enzyme sequence Exo8574. Here we present the biochemical and structural characterization of Exo8574, a GH9 enzyme that showed activity with the substrate p-nitrophenyl-D-cellobioside (pNPC), consistent with cellobiohydrolase activity. Bioinformatics tools were used to perform phylogeny studies of Exo8574 and to identify conserved families and domains. Exo8574 showed 48.8 % homology to a protein from a bacterium belonging to the phylum Firmicutes. The high-quality three-dimensional (3D) model of Exo8574 was obtained by protein structure prediction AlphaFold 2, a neural network-based method. After the heterologous expression of Exo8574 and its purification, biochemical experiments showed that the optimal activity of the enzyme was at a temperature of 55 ºC and pH 6.0, which was enhanced in the presence of metal ions, especially Fe. The estimated kinetic parameters of Exo8574 using the synthetic substrate p-nithrophenyl-beta-D-cellobioside (pNPC) were: V = 9.14 ± 0.2 x10 μmol/min and K = 248.27 ± 26.35 μmol/L. The thermostability test showed a 50 % loss of activity after 1 h incubation at 55 °C. The secondary structure contents of Exo8574 evaluated by Circular Dichroism were pH dependent, with greater structuring of protein in β-antiparallel and α-helices at pH 6.0. The similarity between the CD results and the Ramachandran plot of the 3D model suggests that a reliable model has been obtained. Altogether, the results of the biochemical and structural characterization showed that Exo8574 is capable of acting on p-nithrophenyl-beta-D-cellobioside (pNPC), a substrate that mimics bonds cleaved by cellobiohydrolases. These findings have significant implications for advancing in the field of biomass conversion while also contributing to efforts aimed at overcoming challenges in developing more efficient cellulase cocktails.
28The Termite Fungal Cultivar Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion.PubMed
Felix Schalk, Cene Gostinčar, Nina B Kreuzenbeck, et al.
mBio. 2021 Jun 29;12(3):e0355120. doi: 10.1128/mBio.03551-20. Epub 2021 Jun 15.
Macrotermitine termites have domesticated fungi in the genus as their primary food source using predigested plant biomass. To access the full nutritional value of lignin-enriched plant biomass, the termite-fungus symbiosis requires the depolymerization of this complex phenolic polymer. While most previous work suggests that lignocellulose degradation is accomplished predominantly by the fungal cultivar, our current understanding of the underlying biomolecular mechanisms remains rudimentary. Here, we provide conclusive omics and activity-based evidence that employs not only a broad array of carbohydrate-active enzymes (CAZymes) but also a restricted set of oxidizing enzymes (manganese peroxidase, dye decolorization peroxidase, an unspecific peroxygenase, laccases, and aryl-alcohol oxidases) and Fenton chemistry for biomass degradation. We propose for the first time that induces hydroquinone-mediated Fenton chemistry (Fe + HO + H → Fe + OH + HO) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MHQ, compound 19)-based electron shuttle system to complement the enzymatic degradation pathways. This study provides a comprehensive depiction of how efficient biomass degradation by means of this ancient insect's agricultural symbiosis is accomplished. Fungus-growing termites have optimized the decomposition of recalcitrant plant biomass to access valuable nutrients by engaging in a tripartite symbiosis with complementary contributions from a fungal mutualist and a codiversified gut microbiome. This complex symbiotic interplay makes them one of the most successful and important decomposers for carbon cycling in Old World ecosystems. To date, most research has focused on the enzymatic contributions of microbial partners to carbohydrate decomposition. Here, we provide genomic, transcriptomic, and enzymatic evidence that also employs redox mechanisms, including diverse ligninolytic enzymes and a Fenton chemistry-based hydroquinone-catalyzed lignin degradation mechanism, to break down lignin-rich plant material. Insights into these efficient decomposition mechanisms reveal new sources of efficient ligninolytic agents applicable for energy generation from renewable sources.
29The Core Gut Microbiome of the American Cockroach, Periplaneta americana, Is Stable and Resilient to Dietary Shifts.PubMed
Kara A Tinker, Elizabeth A Ottesen
Appl Environ Microbiol. 2016 Oct 27;82(22):6603-6610. doi: 10.1128/AEM.01837-16. Print 2016 Nov 15.
UNLABELLED: The omnivorous cockroach Periplaneta americana hosts a diverse hindgut microbiota encompassing hundreds of microbial species. In this study, we used 16S rRNA gene sequencing to examine the effect of diet on the composition of the P. americana hindgut microbial community. Results show that the hindgut microbiota of P. americana exhibit a highly stable core microbial community with low variance in compositions between individuals and minimal community change in response to dietary shifts. This core hindgut microbiome is shared between laboratory-hosted and wild-caught individuals, although wild-caught specimens exhibited a higher diversity of low-abundance microbes that were lost following extended cultivation under laboratory conditions. This taxonomic stability strongly contrasts with observations of the gut microbiota of mammals, which have been shown to be highly responsive to dietary change. A comparison of P. americana hindgut samples with human fecal samples indicated that the cockroach hindgut community exhibited higher alpha diversity but a substantially lower beta diversity than the human gut microbiome. This suggests that cockroaches have evolved unique mechanisms for establishing and maintaining a diverse and stable core microbiome. IMPORTANCE: The gut microbiome plays an important role in the overall health of its host. A healthy gut microbiota typically assists with defense against pathogens and the digestion and absorption of nutrients from food, while dysbiosis of the gut microbiota has been associated with reduced health. In this study, we examined the composition and stability of the gut microbiota from the omnivorous cockroach Periplaneta americana. We found that P. americana hosts a diverse core gut microbiome that remains stable after drastic long-term changes in diet. While other insects, notably ant and bee species, have evolved mechanisms for maintaining a stable association with specific gut microbiota, these insects typically host low-diversity gut microbiomes and consume specialized diets. In contrast, P. americana hosts a gut microbiota that is highly species rich and consumes a diverse solid diet, suggesting that cockroaches have evolved unique mechanisms for developing and maintaining a stable gut microbiota.
30Diet Influences the Gut Microbial Diversity and Olfactory Preference of the German Cockroach Blattella germanica.PubMed
Jian Zhu, Yinghua Wu, Fei Lin, et al.
Curr Microbiol. 2022 Dec 2;80(1):23. doi: 10.1007/s00284-022-03123-w.
The gut microbiota of insects has been proven to play a role in the host's nutrition and foraging. The German cockroach, Blattella germanica, is an important vector of various pathogens and causes severe allergic reactions in humans. Food bait is an effective and frequently used method of controlling this omnivorous insect. Thus, understanding the relationships among diet, gut microbiota, and olfactory preferences could be useful for optimizing this management strategy. In this study, B. germanica was exposed to different foods, i.e., high-fat diet, high-protein diet, high-starch diet, and dog food (as control). Then their gut microbial and olfactory responses were investigated. 16S rRNA gene sequencing confirmed that the gut microbiota significantly differed across the four treatments, especially in relation to bacteria associated with the metabolism and digestion of essential components. Behavioral tests and the antenna electrophysiological responses showed that insects had a greater preference for other types of diets compared with their long-term domesticated diet. Moreover, continuously providing a single-type diet could change almost all the OR genes' expression of B. germanica, especially BgORco, which was significantly repressed compared to control. These results indicate that diet can shape the gut microbiota diversity and drive the olfactory preference of B. germanica. The association between gut microbiota profiles and diets can be utilized in managing B. germanica according to their olfactory preference.
31Diet is not the primary driver of bacterial community structure in the gut of litter-feeding cockroaches.PubMed
Niclas Lampert, Aram Mikaelyan, Andreas Brune
BMC Microbiol. 2019 Oct 30;19(1):238. doi: 10.1186/s12866-019-1601-9.
BACKGROUND: Diet is a major determinant of bacterial community structure in termite guts, but evidence of its importance in the closely related cockroaches is conflicting. Here, we investigated the ecological drivers of the bacterial gut microbiota in cockroaches that feed on lignocellulosic leaf litter. RESULTS: The physicochemical conditions determined with microsensors in the guts of Ergaula capucina, Pycnoscelus surinamensis, and Byrsotria rothi were similar to those reported for both wood-feeding and omnivorous cockroaches. All gut compartments were anoxic at the center and showed a slightly acidic to neutral pH and variable but slightly reducing conditions. Hydrogen accumulated only in the crop of B. rothi. High-throughput amplicon sequencing of bacterial 16S rRNA genes documented that community structure in individual gut compartments correlated strongly with the respective microenvironmental conditions. A comparison of the hindgut microbiota of cockroaches and termites from different feeding groups revealed that the vast majority of the core taxa in cockroaches with a lignocellulosic diet were present also in omnivorous cockroaches but absent in wood-feeding higher termites. CONCLUSION: Our results indicate that diet is not the primary driver of bacterial community structure in the gut of wood- and litter-feeding cockroaches. The high similarity to the gut microbiota of omnivorous cockroaches suggests that the dietary components that are actually digested do not differ fundamentally between feeding groups.
32Microbial colonization promotes model cockroach gut tissue growth and development.PubMed
Benjamin C Jahnes, Keyshap Poudel, Amelia M Staats, et al.
J Insect Physiol. 2021 Aug-Sep;133:104274. doi: 10.1016/j.jinsphys.2021.104274. Epub 2021 Jul 1.
BACKGROUND: Digestive tissues are essential for diet processing and nutrient accessibility, especially in omnivores, and these functions occur despite and in collaboration with dynamic microbial communities that reside within and upon these tissues. Prolonged host development and reduced digestive tissue sizes have been observed in germ-free animals, and normal host phenotypes were recovered following the re-introduction of typical gut microbiomes via coprophagy. RESULTS: High-resolution histological analyses of Periplaneta americana cockroach digestive tissues revealed that total prevention of microbial colonization of the gut had severe impacts on the growth and development of gut tissues, especially the posterior midgut and anterior hindgut subcompartments that are expected to be colonized and inhabited by the greatest number of bacteria. Juveniles that were briefly exposed to normal gut microbiota exhibited a partial gut morphological recovery, suggesting that a single inoculation was insufficient. These data highlight gut microbiota as integral to normal growth and development of tissues they are in direct contact with and, more broadly, the organism in which they reside. CONCLUSIONS: We draw on these data, host life history traits (i.e. multigenerational cohousing, molting, and filial coprophagy and exuvia feeding), and previous studies to suggest a host developmental model in which gut tissues reflect a conflict-collaboration dynamic where 1) nutrient-absorptive anterior midgut tissues are in competition with transient and resident bacteria for easily assimilable dietary nutrients and whose growth is least-affected by the presence of gut bacteria and 2) posterior midgut, anterior hindgut, and to a lesser degree, posterior hindgut tissues are significantly impacted by gut bacterial presence because they are occupied by the greatest number of bacteria and the host is relying upon, and thus collaborating with, them to assist with complex polysaccharide catabolism processing and nutrient provisioning (i.e. short-chain fatty acids).
33Phylosymbiosis across Deeply Diverging Lineages of Omnivorous Cockroaches (Order Blattodea).PubMed
Kara A Tinker, Elizabeth A Ottesen
Appl Environ Microbiol. 2020 Mar 18;86(7). doi: 10.1128/AEM.02513-19.
The gut microbiome is shaped by both host diet and host phylogeny. However, separating the relative influence of these two factors over long periods of evolutionary time is often difficult. We conducted a 16S rRNA gene amplicon-based survey of the gut microbiome from 237 individuals and 19 species of omnivorous cockroaches from the order Blattodea. The order Blattodea represents an ancient lineage of insects that emerged over 300 million years ago, have a diverse gut microbiota, and have a typically gregarious lifestyle. All cockroaches shared a broadly similar gut microbiota, with 66 microbial families present across all species and 13 present in every individual examined. Although our network analysis of the cockroach gut microbiome showed a large amount of connectivity, we demonstrated that gut microbiota cluster strongly by host species. We conducted follow-up tests to determine if cockroaches exhibit phylosymbiosis, or the tendency of host-associated microbial communities to parallel the phylogeny of related host species. Across the full data set, gut microbial community similarity was not found to correlate with host phylogenetic distance. However, a weak but significant phylosymbiotic signature was observed using the matching cluster metric, which allows for localized changes within a phylogenetic tree that are more likely to occur over long evolutionary distances. This finding suggests that host phylogeny plays a large role in structuring the cockroach gut microbiome over shorter evolutionary distances and a weak but significant role in shaping the gut microbiome over extended periods of evolutionary time. The gut microbiome plays a key role in host health. Therefore, it is important to understand the evolution of the gut microbiota and how it impacts, and is impacted by, host evolution. In this study, we explore the relationship between host phylogeny and gut microbiome composition in omnivorous, gregarious cockroaches within the Blattodea order, an ancient lineage that spans 300 million years of evolutionary divergence. We demonstrate a strong relationship between host species identity and gut microbiome composition and found a weaker but significant role for host phylogeny in determining microbiome similarity over extended periods of evolutionary time. This study advances our understanding of the role of host phylogeny in shaping the gut microbiome over different evolutionary distances.
34Dispersion and colonisation by fungus-growing termites: Vertical transmission of the symbiont helps, but then...?PubMed
Tania Nobre, Durr K Aanen
Commun Integr Biol. 2010 May;3(3):248-50. doi: 10.4161/cib.3.3.11415.
The fungus-growing termites (Macrotermitinae) have developed an obligate mutualistic symbiosis with fungi (Termitomyces) and, in most cases, the symbiotic partner is collected from the environment upon establishment of a new colony (horizontal transmission). The requirement that partners are able to find and recognize each other after independent reproduction is likely to severely constrain long distance dispersal. In support of this hypothesis, we have recently shown that a single colonisation of Madagascar by fungus-growing termites has occurred. The successful colonizers belong to the genus Microtermes, known to inherit their symbiont from the parental colony (vertical transmission). However, the fungal symbionts of Madagascar were not monophyletic, as expected under strict vertical transmission. Here we further discuss these findings, and we suggest further bottlenecks to dispersion and propose a transient window for horizontal transmission for the otherwise vertically transmitted Termitomyces strains.
35Presumptive horizontal symbiont transmission in the fungus-growing termite Macrotermes natalensis.PubMed
H H de Fine Licht, J J Boomsma, D K Aanen
Mol Ecol. 2006 Oct;15(11):3131-8. doi: 10.1111/j.1365-294X.2006.03008.x.
All colonies of the fungus-growing termite Macrotermes natalensis studied so far are associated with a single genetically variable lineage of Termitomyces symbionts. Such limited genetic variation of symbionts and the absence of sexual fruiting bodies (mushrooms) on M. natalensis mounds would be compatible with clonal vertical transmission, as is known to occur in Macrotermes bellicosus. We investigated this hypothesis by analysing DNA sequence polymorphisms as codominant SNP markers of four single-copy gene fragments of Termitomyces isolates from 31 colonies of M. natalensis. A signature of free recombination was found, indicative of frequent sexual horizontal transmission. First, all 31 strains had unique multilocus genotypes. Second, SNP markers (n = 55) were largely in Hardy-Weinberg equilibrium (90.9%) and almost all possible pairs of SNPs between genetically unlinked loci were in linkage equilibrium (96.7%). Finally, extensive intragenic recombination was found, especially in the EF1alpha fragment. Substantial genetic variation and a freely recombining population structure can only be explained by frequent horizontal and sexual transmission of Termitomyces. The apparent variation in symbiont transmission mode among Macrotermes species implies that vertical symbiont transmission can evolve rapidly. The unexpected finding of horizontal transmission makes the apparent absence of Termitomyces mushrooms on M. natalensis mounds puzzling. To our knowledge, this is the first detailed study of the genetic population structure of a single lineage of Termitomyces.
36Alarm communication predates eusociality in termites.PubMed
David Sillam-Dussès, Vojtěch Jandák, Petr Stiblik, et al.
Commun Biol. 2023 Jan 21;6(1):83. doi: 10.1038/s42003-023-04438-5.
Termites (Blattodea: Isoptera) have evolved specialized defensive strategies for colony protection. Alarm communication enables workers to escape threats while soldiers are recruited to the source of disturbance. Here, we study the vibroacoustic and chemical alarm communication in the wood roach Cryptocercus and in 20 termite species including seven of the nine termite families, all life-types, and all feeding and nesting habits. Our multidisciplinary approach shows that vibratory alarm signals represent an ethological synapomorphy of termites and Cryptocercus. In contrast, chemical alarms have evolved independently in several cockroach groups and at least twice in termites. Vibroacoustic alarm signaling patterns are the most complex in Neoisoptera, in which they are often combined with chemical signals. The alarm characters correlate to phylogenetic position, food type and hardness, foraging area size, and nesting habits. Overall, species of Neoisoptera have developed the most sophisticated communication system amongst termites, potentially contributing to their ecological success.
37Termites assess wood size by using vibration signals.PubMed
Theodore A Evans, Joseph C S Lai, Emilie Toledano, et al.
Proc Natl Acad Sci U S A. 2005 Mar 8;102(10):3732-7. doi: 10.1073/pnas.0408649102. Epub 2005 Feb 25.
Contrary to the common perception that termites are indiscriminant eaters, termites choose their food carefully; however, the methods by which they choose food are not well understood. Using choice experiments and recordings of termites feeding on wooden blocks of different sizes, we show that worker drywood termites (Cryptotermes domesticus) use the resonant frequency of a block of wood to assess its size. Drywood termites showed differences in their response to vibration recordings of termites compared with artificially generated signals, suggesting that they can discriminate the source of vibration. Furthermore, fewer workers matured into neotenic reproductives when recorded termite signals were played, suggesting that vibration signals play an important role in termite communication.
38Termites eavesdrop to avoid competitors.PubMed
Theodore A Evans, Ra Inta, Joseph C S Lai, et al.
Proc Biol Sci. 2009 Nov 22;276(1675):4035-41. doi: 10.1098/rspb.2009.1147. Epub 2009 Aug 26.
Competition exclusion, when a single species dominates resources due to superior competitiveness, is seldom observed in nature. Termites compete for resources with deadly consequences, yet more than one species can be found feeding in the same wooden resource. This is especially surprising when drywood species, with colonies of a few hundred, are found cohabiting with subterranean species, with colonies of millions. Termites communicate vibro-acoustically and, as these signals can travel over long distances, they are vulnerable to eavesdropping. We investigated whether drywood termites could eavesdrop on vibration cues from subterranean species. We show, using choice experiments and recordings, that the drywood termite Cryptotermes secundus can distinguish its own species from the dominant competitor in the environment, the subterranean termite Coptotermes acinaciformis. The drywood termite was attracted to its own vibration cues, but was repelled by those of the subterranean species. This response increased with decreasing wood size, corresponding with both increased risk and strength of the cue. The drywood termites appear to avoid confrontation by eavesdropping on the subterranean termites; these results provide further evidence that vibro-acoustic cues are important for termite sensory perception and communication.
39Vibrational long-distance communication in the termites Macrotermes natalensis and Odontotermes sp.PubMed
Felix A Hager, Wolfgang H Kirchner
J Exp Biol. 2013 Sep 1;216(Pt 17):3249-56. doi: 10.1242/jeb.086991.
Fungus-growing higher termites build long subterranean galleries that lead outwards from the nest to foraging sites. When soldiers are disturbed, they tend to drum with their heads against the substrate and thereby create vibrational alarm signals. The present study aimed at describing these acoustic signals, how they are elicited, produced and perceived, and how these signals propagate within the galleries and nests over long distances in two termite species of the Southern African savannah, Macrotermes natalensis and an Odontotermes sp. The signals consist of trains of pulses with a pulse repetition rate of 10-20 Hz. The galleries have physical features that promote vibrational communication and are used as channels for long-distance communication. In M. natalensis, the signal propagation velocity is ~130 m s(-1) and the signals are attenuated by ~0.4 dB per centimetre distance. Nestmates are extremely sensitive to these vibrations with a behavioural threshold amplitude of 0.012 m s(-2). Workers respond by a fast retreat into the nest and soldiers are recruited to the source of vibration. Soldiers also start to drum with a reaction time of about 0.3 s, thereby amplifying the intensity of the signal. This social long-distance communication through chains of signal-reamplifying termites results in a relatively slow propagation (1.3 m s(-1)) of the signal without decrement over distances of several metres.
40Reproductives and eggs trigger worker vibration in a subterranean termite.PubMed
Fanny Ruhland, Marion Moulin, Marina Choppin, et al.
Ecol Evol. 2020 Jun 7;10(12):5892-5898. doi: 10.1002/ece3.6325. eCollection 2020 Jun.
In insect societies, the presence of reproductives or eggs has been shown to shape several biological traits in the colony members. Social interactions are one of these traits that involve modification of the communication system of the entire colony. Many studies described the role of chemical compounds and dominance behaviors in the presence of reproductive but vibratory behaviors received very few investigations. Yet, vibratory behaviors are ideal candidates, particularly for subterranean species like termites, as they could be quickly transmitted through the substrate and could be very diversified (origin, modulation). Here, we investigated whether the presence of reproductives/eggs affects the vibratory behavior (body-shaking) of workers in the subterranean termite . Our results reveal that the presence of reproductives or eggs triggers an increase of workers' body-shaking, independent of their colony of origin after 24 hr. We hypothesize that vibratory communication could be used to transfer information about the presence of reproductives and eggs to the entire colony, suggesting that vibratory behaviors could serve as an important yet neglected mediator of social regulation.
41Vibratory behaviour produces different vibrations patterns in presence of reproductives in a subterranean termite species.PubMed
Louis Pailler, Samuel Desvignes, Fanny Ruhland, et al.
Sci Rep. 2021 May 10;11(1):9902. doi: 10.1038/s41598-021-88292-7.
Vibratory behaviours are widespread in social insects, but the produced vibrations remain poorly explored. Communication using vibrations is an efficient way to transmit information in subterranean environments where visual and odorant signals are less efficient. In termites, different vibratory behaviours are performed in different contexts like reproductive regulation and alarm signalling, but only few studies explored the structure of the produced vibrations (i.e., duration, number of pulses, amplitude). Here, we described several types of vibrations produced by a vibratory behaviour widespread in termites (body-shaking), which can be transmitted through the substrate and detected by other colony members. We analysed the structures of the emitted vibrations and the occurrence of the body-shaking events in presence/absence of reproductives and/or in presence/absence of a stress stimuli (flashlight) in the subterranean termite Reticulitermes flavipes. Interestingly, only the presence of the reproductives did influence the number of pulses and the duration of the emitted vibrations. Moreover, the first part of the emitted vibrations seems to be enough to encode reproductive information, but other parts might hold other type of information. Body-shaking occurrence did increase in presence of reproductives but only briefly under a flashlight. These results show that vibratory cues are complex in termites and their diversity might encode a plurality of social cues.
42Exploring the Caste-Specific Multi-Layer Defense Mechanism of Formosan Subterranean Termites, Coptotermes formosanus Shiraki.PubMed
Abid Hussain, Ming-Yi Tian, Shuo-Yang Wen
Int J Mol Sci. 2017 Dec 12;18(12):2694. doi: 10.3390/ijms18122694.
The survival and foraging of Shiraki in a microbe-rich environment reflect the adaptation of an extraordinary, sophisticated defense mechanism by the nest-mates. We aimed to explore the host pathogen interaction by studying caste-specific volatile chemistry and genes encoding the antioxidant defense of winged imagoes, nymphs, soldiers and workers of Formosan subterranean termites. Qualitative analyses of Shiraki performed by HS-SPME/GC-MS showed considerable variations in the chemical composition of volatile organic compounds (VOCs) and their proportions among all the castes. Winged imagoes produced the most important compounds such as naphthalene and hexanoic acid. The antifungal activity of these compounds along with nonanal, -pentadecane, tetradecane, -heptadecane and methyl octanoate against the conidial suspensions of and isolates enable us to suggest that the failure of natural fungal infection in the nest is due to the antiseptic environment of the nest, which is mainly controlled by the VOCs of nest-mates. In addition, conidial germination of and isolates evaluated on the cuticle of each caste showed significant variations among isolates and different castes. Our results showed that the conidia of 02049 exhibited the highest germination on the cuticle of all the inoculated castes. Moreover, we recorded the lowest germination of the conidia of 200436. Caste-specific germination variations enabled us to report for the first time that the cuticle of winged imagoes was found to be the most resistant cuticle. The analysis of the transcriptome of Shiraki revealed the identification of 17 genes directly involved in antioxidant defense. Expression patterns of the identified antioxidant genes by quantitative real-time PCR (qPCR) revealed the significantly highest upregulation of , , , , , , , , and genes among winged imagoes upon infection with the most virulent isolate, 02049. Furthermore, soldiers showed the least expression of genes encoding antioxidant defense. Our findings indicated that the volatile chemistry of nest-mates and genes encoding antioxidant defense greatly contribute to the survival and foraging of Formosan subterranean termites in a microbe-rich habitat.
43The ability of lizards to identify an artificial Batesian mimic.PubMed
Josef Beneš, Petr Veselý
Zoology (Jena). 2017 Aug;123:46-52. doi: 10.1016/j.zool.2017.05.010. Epub 2017 Jun 3.
Birds are usually considered the main predators shaping the evolution of aposematic signals and mimicry. Nevertheless, some lizards also represent predominately visually oriented predators, so they may also play an important role in the evolution of aposematism. Despite this fact, experimental evidence regarding the responses of lizards to aposematic prey is very poor compared to such evidence in birds. Lizards possess very similar sensory and cognitive abilities to those of birds and their response to aposematic prey may thus be affected by very similar processes. We investigated the reactions of a lizard, the Gran Canaria skink (Chalcides sexlineatus), to an aposematic prey and its artificial Batesian mimic. Further, we attempted to ascertain whether the lizard's food experience has any effect on its ability to recognise an artificial Batesian mimic, by using two groups of predators differing in their prior experience with the prey from which the mimic was fabricated. The red firebug (Pyrrhocoris apterus) was used as an aposematic model, and the Guyana spotted roach (Blaptica dubia) as the palatable prey from which the mimic was fabricated. The appearance of the roach was modified by a paper sticker placed on its back. The skinks showed a strong aversion towards the model firebug. They also avoided attacking the cockroaches with the firebug pattern sticker. This suggests that a visual rather than a chemical signal is responsible for this aversion. The protection provided by the firebug sticker was even effective when the skinks were familiar with unmodified cockroaches (previous food experience).
44The soldiers in societies: defense, regulation, and evolution.PubMed
Li Tian, Xuguo Zhou
Int J Biol Sci. 2014 Mar 5;10(3):296-308. doi: 10.7150/ijbs.6847. eCollection 2014.
The presence of reproductively altruistic castes is one of the primary traits of the eusocial societies. Adaptation and regulation of the sterile caste, to a certain extent, drives the evolution of eusociality. Depending on adaptive functions of the first evolved sterile caste, eusocial societies can be categorized into the worker-first and soldier-first lineages, respectively. The former is marked by a worker caste as the first evolved altruistic caste, whose primary function is housekeeping, and the latter is highlighted by a sterile soldier caste as the first evolved altruistic caste, whose task is predominantly colony defense. The apparent functional differences between these two fundamentally important castes suggest worker-first and soldier-first eusociality are potentially driven by a suite of distinctively different factors. Current studies of eusocial evolution have been focused largely on the worker-first Hymenoptera, whereas understanding of soldier-first lineages including termites, eusocial aphids, gall-dwelling thrips, and snapping shrimp, is greatly lacking. In this review, we summarize the current state of knowledge on biology, morphology, adaptive functions, and caste regulation of the soldier caste. In addition, we discuss the biological, ecological and genetic factors that might contribute to the evolution of distinct caste systems within eusocial lineages.
45Social Immunity: Emergence and Evolution of Colony-Level Disease Protection.PubMed
Sylvia Cremer, Christopher D Pull, Matthias A Fürst
Annu Rev Entomol. 2018 Jan 7;63:105-123. doi: 10.1146/annurev-ento-020117-043110. Epub 2017 Sep 25.
Social insect colonies have evolved many collectively performed adaptations that reduce the impact of infectious disease and that are expected to maximize their fitness. This colony-level protection is termed social immunity, and it enhances the health and survival of the colony. In this review, we address how social immunity emerges from its mechanistic components to produce colony-level disease avoidance, resistance, and tolerance. To understand the evolutionary causes and consequences of social immunity, we highlight the need for studies that evaluate the effects of social immunity on colony fitness. We discuss the roles that host life history and ecology have on predicted eco-evolutionary dynamics, which differ among the social insect lineages. Throughout the review, we highlight current gaps in our knowledge and promising avenues for future research, which we hope will bring us closer to an integrated understanding of socio-eco-evo-immunology.
46Cuticular nitrogen economy during development in the cockroach Cryptocercus punctulatus and the termite Neotermes jouteli.PubMed
D E Mullins, C A Nalepa, A J Mullins, et al.
J Insect Physiol. 2025 Jan;160:104745. doi: 10.1016/j.jinsphys.2024.104745. Epub 2024 Dec 25.
The role of nitrogen during insect development and reproduction is key in the success of a species, and is of primary importance in wood feeding taxa. Based on comparison of xylophagous, one-piece termites to the termite sister group, subsocial wood-feeding cockroaches in the genus Cryptocercus, it has been proposed that the evolution of termite eusociality involved a fundamental shift in nitrogen allocation strategies. Cryptocercus exhibits a nitrogen storage economy, with individuals gradually increasing in size and cuticular density over a years-long developmental period. Termites, however, remain in a juvenilized morphotype with minimal investment into cuticle, suggesting that nitrogen is conserved and circulated according to the needs of the colony via behaviors such as trophallaxis and cannibalism. We examined the nitrogen economy of Cryptocercus punctulatus and the dampwood termite Neotermes jouteli, focusing on cuticular nitrogen investment during development and exuvial nitrogen losses resulting from molting. Cryptocercus progressively changes from a pale, thin, soft cuticle at hatch to a dark, thick, heavily sclerotized cuticle in adults; increases in N/mg cuticle and the quantity of cuticular catecholamines are correlated with these ontogenetic color changes. There were significant differences in the nitrogen content of two successive age classes of early stage juveniles and in their discarded exuvia at molt. Soldier and alate castes of N. jouteli exhibited the highest sclerotization/melanization indices; pseudergates had levels comparable to those measured in Class I (3rd and 4th instar) juveniles of C. punctulatus. Exuvia of N. jouteli contained 0.19 μgN/mg, while exuvia of approximately two- and three-year-old C. punctulatus had 72.9 and 82.6 μgN/mg, respectively. Our data support the hypothesis that the evolution of termite eusociality from subsocial cockroach ancestors was rooted in chronic fitness limitations imposed by their low nitrogen diet.
47Trophic Path of Marked Exuviae Within Colonies of Coptotermes gestroi (Blattodea: Rhinotermitidae).PubMed
Reina L Tong, Eun-Kyung Choi, Kelly Ugarelli, et al.
J Insect Sci. 2023 Mar 1;23(2). doi: 10.1093/jisesa/iead007.
Nitrogen, a limiting growth factor in wood-feeding insects, was hypothesized to play a role in the recently discovered behavior of subterranean termites returning to the nest to molt. Coptotermes gestroi (Wasmann) exuviae is approximately 11% N by dry weight, and therefore a potentially rich source of recyclable nitrogen. Exuviae from a C. gestroi colony were marked with immunoglobulin G (IgG) and were fed to two-year-old C. gestroi colonies. IgG-marked exuviae were detected with an enzyme-linked immunosorbent assay. The IgG marker was later detected in every caste and life stage except first-instar larvae (L1). The proportion of individuals positive for the marker varied by caste, with the queens always being positive for the marker. The queens and second-or-higher-instar workers (W2+) had significantly higher concentrations of the marker than the eggs and L1. The trophic path of exuviae includes individuals that directly fed on marked exuviae (workers and possibly second-instar larvae) and individuals that secondarily received marked exuviae through trophallaxis (queens, kings, and soldiers). This study described the trophic path of consumed exuviae and demonstrated its role in the recycling of nitrogen in a subterranean termite. Molting at the central nest may be an efficient means to transfer nitrogen from shed exuviae to recipients and may be a nitrogen recycling behavior conserved from a termite ancestor.
48Genome Evolution and Nitrogen Fixation in Bacterial Ectosymbionts of a Protist Inhabiting Wood-Feeding Cockroaches.PubMed
Vera Tai, Kevin J Carpenter, Peter K Weber, et al.
Appl Environ Microbiol. 2016 Jul 15;82(15):4682-4695. doi: 10.1128/AEM.00611-16. Print 2016 Aug 1.
UNLABELLED: By combining genomics and isotope imaging analysis using high-resolution secondary ion mass spectrometry (NanoSIMS), we examined the function and evolution of Bacteroidales ectosymbionts of the protist Barbulanympha from the hindguts of the wood-eating cockroach Cryptocercus punctulatus In particular, we investigated the structure of ectosymbiont genomes, which, in contrast to those of endosymbionts, has been little studied to date, and tested the hypothesis that these ectosymbionts fix nitrogen. Unlike with most obligate endosymbionts, genome reduction has not played a major role in the evolution of the Barbulanympha ectosymbionts. Instead, interaction with the external environment has remained important for this symbiont as genes for synthesis of transporters, outer membrane proteins, lipopolysaccharides, and lipoproteins have been retained. The ectosymbiont genome carried two complete operons for nitrogen fixation, a urea transporter, and a urease, indicating the availability of nitrogen as a driving force behind the symbiosis. NanoSIMS analysis of C. punctulatus hindgut symbionts exposed in vivo to (15)N2 supports the hypothesis that Barbulanympha ectosymbionts are capable of nitrogen fixation. This genomic and in vivo functional investigation of protist ectosymbionts highlights the diversity of evolutionary forces and trajectories that shape symbiotic interactions. IMPORTANCE: The ecological and evolutionary importance of symbioses is increasingly clear, but the overall diversity of symbiotic interactions remains poorly explored. In this study, we investigated the evolution and nitrogen fixation capabilities of ectosymbionts attached to the protist Barbulanympha from the hindgut of the wood-eating cockroach Cryptocercus punctulatus In addressing genome evolution of protist ectosymbionts, our data suggest that the ecological pressures influencing the evolution of extracellular symbionts clearly differ from intracellular symbionts and organelles. Using NanoSIMS analysis, we also obtained direct imaging evidence of a specific hindgut microbe playing a role in nitrogen fixation. These results demonstrate the power of combining NanoSIMS and genomics tools for investigating the biology of uncultivable microbes. This investigation paves the way for a more precise understanding of microbial interactions in the hindguts of wood-eating insects and further exploration of the diversity and ecological significance of symbiosis between microbes.
49'Candidatus Adiutrix intracellularis', an endosymbiont of termite gut flagellates, is the first representative of a deep-branching clade of Deltaproteobacteria and a putative homoacetogen.PubMed
Wakako Ikeda-Ohtsubo, Jürgen F H Strassert, Tim Köhler, et al.
Environ Microbiol. 2016 Sep;18(8):2548-64. doi: 10.1111/1462-2920.13234. Epub 2016 Apr 21.
Termite gut flagellates are typically colonized by specific bacterial symbionts. Here we describe the phylogeny, ultrastructure and subcellular location of 'Candidatus Adiutrix intracellularis', an intracellular symbiont of Trichonympha collaris in the termite Zootermopsis nevadensis. It represents a novel, deep-branching clade of uncultured Deltaproteobacteria widely distributed in intestinal tracts of termites and cockroaches. Fluorescence in situ hybridization and transmission electron microscopy localized the endosymbiont near hydrogenosomes in the posterior part and near the ectosymbiont 'Candidatus Desulfovibrio trichonymphae' in the anterior part of the host cell. The draft genome of 'Ca. Adiutrix intracellularis' obtained from a metagenomic library revealed the presence of a complete gene set encoding the Wood-Ljungdahl pathway, including two homologs of fdhF encoding hydrogenase-linked formate dehydrogenases (FDHH ) and all other components of the recently described hydrogen-dependent carbon dioxide reductase (HDCR) complex, which substantiates previous claims that the symbiont is capable of reductive acetogenesis from CO2 and H2 . The close phylogenetic relationship between the HDCR components and their homologs in homoacetogenic Firmicutes and Spirochaetes suggests that the deltaproteobacterium acquired the capacity for homoacetogenesis via lateral gene transfer. The presence of genes for nitrogen fixation and the biosynthesis of amino acids and cofactors indicate the nutritional nature of the symbiosis.
50Comparative genomics of Blattabacterium cuenoti: the frozen legacy of an ancient endosymbiont genome.PubMed
Rafael Patiño-Navarrete, Andrés Moya, Amparo Latorre, et al.
Genome Biol Evol. 2013;5(2):351-61. doi: 10.1093/gbe/evt011.
Many insect species have established long-term symbiotic relationships with intracellular bacteria. Symbiosis with bacteria has provided insects with novel ecological capabilities, which have allowed them colonize previously unexplored niches. Despite its importance to the understanding of the emergence of biological complexity, the evolution of symbiotic relationships remains hitherto a mystery in evolutionary biology. In this study, we contribute to the investigation of the evolutionary leaps enabled by mutualistic symbioses by sequencing the genome of Blattabacterium cuenoti, primary endosymbiont of the omnivorous cockroach Blatta orientalis, and one of the most ancient symbiotic associations. We perform comparative analyses between the Blattabacterium cuenoti genome and that of previously sequenced endosymbionts, namely those from the omnivorous hosts the Blattella germanica (Blattelidae) and Periplaneta americana (Blattidae), and the endosymbionts harbored by two wood-feeding hosts, the subsocial cockroach Cryptocercus punctulatus (Cryptocercidae) and the termite Mastotermes darwiniensis (Termitidae). Our study shows a remarkable evolutionary stasis of this symbiotic system throughout the evolutionary history of cockroaches and the deepest branching termite M. darwiniensis, in terms of not only chromosome architecture but also gene content, as revealed by the striking conservation of the Blattabacterium core genome. Importantly, the architecture of central metabolic network inferred from the endosymbiont genomes was established very early in Blattabacterium evolutionary history and could be an outcome of the essential role played by this endosymbiont in the host's nitrogen economy.
51Genome economization in the endosymbiont of the wood roach Cryptocercus punctulatus due to drastic loss of amino acid synthesis capabilities.PubMed
Alexander Neef, Amparo Latorre, Juli Peretó, et al.
Genome Biol Evol. 2011;3:1437-48. doi: 10.1093/gbe/evr118. Epub 2011 Nov 16.
Cockroaches (Blattaria: Dictyoptera) harbor the endosymbiont Blattabacterium sp. in their abdominal fat body. This endosymbiont is involved in nitrogen recycling and amino acid provision to its host. In this study, the genome of Blattabacterium sp. of Cryptocercus punctulatus (BCpu) was sequenced and compared with those of the symbionts of Blattella germanica and Periplaneta americana, BBge and BPam, respectively. The BCpu genome consists of a chromosome of 605.7 kb and a plasmid of 3.8 kb and is therefore approximately 31 kb smaller than the other two aforementioned genomes. The size reduction is due to the loss of 55 genes, 23 of which belong to biosynthetic pathways for amino acids. The pathways for the production of tryptophan, leucine, isoleucine/threonine/valine, methionine, and cysteine have been completely lost. Additionally, the genes for the enzymes catalyzing the last steps of arginine and lysine biosynthesis, argH and lysA, were found to be missing and pseudogenized, respectively. These gene losses render BCpu auxotrophic for nine amino acids more than those corresponding to BBge and BPam. BCpu has also lost capacities for sulfate reduction, production of heme groups, as well as genes for several other unlinked metabolic processes, and genes present in BBge and BPam in duplicates. Amino acids and cofactors that are not synthesized by BCpu are either produced in abundance by hindgut microbiota or are provisioned via a copious diet of dampwood colonized by putrefying microbiota, supplying host and Blattabacterium symbiont with the necessary nutrients and thus permitting genome economization of BCpu.
52Maintenance of essential amino acid synthesis pathways in the Blattabacterium cuenoti symbiont of a wood-feeding cockroach.PubMed
Gaku Tokuda, Liam D H Elbourne, Yukihiro Kinjo, et al.
Biol Lett. 2013 Mar 20;9(3):20121153. doi: 10.1098/rsbl.2012.1153. Print 2013 Jun 23.
In addition to harbouring intestinal symbionts, some animal species also possess intracellular symbiotic microbes. The relative contributions of gut-resident and intracellular symbionts to host metabolism, and how they coevolve are not well understood. Cockroaches and the termite Mastotermes darwiniensis present a unique opportunity to examine the evolution of spatially separated symbionts, as they harbour gut symbionts and the intracellular symbiont Blattabacterium cuenoti. The genomes of B. cuenoti from M. darwiniensis and the social wood-feeding cockroach Cryptocercus punctulatus are each missing most of the pathways for the synthesis of essential amino acids found in the genomes of relatives from non-wood-feeding hosts. Hypotheses to explain this pathway degradation include: (i) feeding on microbes present in rotting wood by ancestral hosts; (ii) the evolution of high-fidelity transfer of gut microbes via social behaviour. To test these hypotheses, we sequenced the B. cuenoti genome of a third wood-feeding species, the phylogenetically distant and non-social Panesthia angustipennis. We show that host wood-feeding does not necessarily lead to degradation of essential amino acid synthesis pathways in B. cuenoti, and argue that ancestral high-fidelity transfer of gut microbes best explains their loss in strains from M. darwiniensis and C. punctulatus.
53The transition path from female workers to neotenic reproductives in the termite Reticulitermes labralis.PubMed
Xiaohong Su, Xiaojuan Yang, Jing Li, et al.
Evol Dev. 2017 Jul;19(4-5):218-226. doi: 10.1111/ede.12229.
Termite workers are characterized by unique flexibility in that a worker can develop in one of three ways: remain a worker, become a soldier within two successive moults, or become a neotenic reproductive (NR) within a single moult. However, is it true that workers can transform into NRs within a single moult? Actually, the developmental pathways of workers turning into NRs remains unclear. In this study, we show for the first time that the female workers of Reticulitermes labralis develop into NRs after a pre-NRs stage. We found that a female worker became a NR after two successive moults, whereas the male workers copulated directly with queens without undergoing any moults. After the first moult led the female workers into the pre-NR stage, the length of their abdomens, seventh sternites and ovaries significantly increased. After the second moult from the pre-NRs stage into NRs, the follicle cells returned to normal, and a few oocytes and follicle cells underwent apoptosis. These results demonstrated that the female pre-NR type was a transitional type during the development of female workers to the NR caste, and the starting point for oogenesis resumption was the NR stage. We confirmed there were fundamental differences in the reproductive pathway of the male and female workers. Therefore, we determined that the transformation process of the female NRs from workers may be a very complex process, and the reproductive biology of the workers has great potential to provide important and spectacular insights into the evolution strategy of termites.
54Life history and development--a framework for understanding developmental plasticity in lower termites.PubMed
Judith Korb, Klaus Hartfelder
Biol Rev Camb Philos Soc. 2008 Aug;83(3):295-313. doi: 10.1111/j.1469-185x.2008.00044.x.
Termites (Isoptera) are the phylogenetically oldest social insects, but in scientific research they have always stood in the shadow of the social Hymenoptera. Both groups of social insects evolved complex societies independently and hence, their different ancestry provided them with different life-history preadaptations for social evolution. Termites, the 'social cockroaches', have a hemimetabolous mode of development and both sexes are diploid, while the social Hymenoptera belong to the holometabolous insects and have a haplodiploid mode of sex determination. Despite this apparent disparity it is interesting to ask whether termites and social Hymenoptera share common principles in their individual and social ontogenies and how these are related to the evolution of their respective social life histories. Such a comparison has, however, been much hampered by the developmental complexity of the termite caste system, as well as by an idiosyncratic terminology, which makes it difficult for non-termitologists to access the literature. Here, we provide a conceptual guide to termite terminology based on the highly flexible caste system of the "lower termites". We summarise what is known about ultimate causes and underlying proximate mechanisms in the evolution and maintenance of termite sociality, and we try to embed the results and their discussion into general evolutionary theory and developmental biology. Finally, we speculate about fundamental factors that might have facilitated the unique evolution of complex societies in a diploid hemimetabolous insect taxon. This review also aims at a better integration of termites into general discussions on evolutionary and developmental biology, and it shows that the ecology of termites and their astounding phenotypic plasticity have a large yet still little explored potential to provide insights into elementary evo-devo questions.
55Regulation of polyphenic caste differentiation in the termite Reticulitermes flavipes by interaction of intrinsic and extrinsic factors.PubMed
Michael E Scharf, Caitlin E Buckspan, Traci L Grzymala, et al.
J Exp Biol. 2007 Dec;210(Pt 24):4390-8. doi: 10.1242/jeb.010876.
Polyphenism is a key strategy used by solitary insects to adapt to changing environmental conditions and by eusocial insects for existing collaboratively in a social environment. In social insects, the morphogenetic juvenile hormone (JH) is often involved in directing the differentiation of polyphenic behavioral castes. The present study examines the effects of JH, environment and feeding on caste polyphenism in a eusocial insect, the termite Reticulitermes flavipes (Kollar). Our approach included a combination of model JH bioassays, SDS-PAGE and western blotting. Our findings revealed significant temperature-dependent effects on (1) JH-induced soldier caste differentiation, (2) abundance of soldier-inhibitory hexamerin proteins, and (3) JH-sequestration by hexamerin proteins. Additionally, though it appears to be dependent on a complex interaction of factors, feeding apparently plays a significant upstream role in enhancing hexamerin accumulation under normal colony conditions. These findings offer important new information on termite eusocial polyphenism by providing the first mechanistic evidence linking an intrinsic caste regulatory factor (hexamerin proteins) to an upstream extrinsic factor (environment) and a downstream response (caste differentiation). These observations are consistent with the hypothesis that the hexamerins serve as an environmentally and nutritionally responsive switching mechanism that regulates termite caste polyphenism.
56Molting in workers of the Formosan subterranean termite Coptotermes formosanus.PubMed
Ashok Raina, Yong Ihl Park, Dale Gelman
J Insect Physiol. 2008 Jan;54(1):155-61. doi: 10.1016/j.jinsphys.2007.08.015. Epub 2007 Sep 8.
The Formosan subterranean termite, Coptotermes formosanus, with its huge colonies, is a major urban pest in several southern states and Hawaii as well as in South Asia. Because of their cryptic nature (underground habitat) and very long life cycle, not much is known about molting in termite workers. In C. formosanus, the workers stop foraging and lose their gut fauna, respectively, approximately 10 and 5 days prior to ecdysis. In any given colony an average of 1.01% (range 0.6-1.8) of the workers were found to molt each day under laboratory conditions. Workers destined to molt become sluggish and their head capsules develop a mottled texture one day prior to ecdysis. Ecdysis was generally accomplished with the assistance of other workers, which also fed on the exuviae. Immediately after molting worker mandibles were light pink in color and became fully melanized approximately two days later. Gut fauna were acquired on the fourth day after molting. Flagellates were transferred as small encysted cells from other workers through proctodeal feeding. Juvenile hormone III titer ranged between 30-41 pg/mg bodyweight in all stages except in workers sampled 6 days prior to ecdysis. In these workers the titer was 80.5 pg/mg. The high juvenile hormones (JH) titer may also be involved in causing defaunation. Ecdysteroid titer increased from 2.1 pg/mg in non-molting workers to 359.5 and 332.4 pg/mg one and two days following defaunation, respectively. There was a second smaller peak two days prior to ecdysis.
57Body part-specific development in termite caste differentiation: crosstalk between hormonal actions and developmental toolkit genes.PubMed
Kohei Oguchi, Toru Miura
Curr Opin Insect Sci. 2024 Jun;63:101183. doi: 10.1016/j.cois.2024.101183. Epub 2024 Feb 29.
In social insects, interactions among colony members trigger caste differentiation with morphological modifications. During caste differentiation in termites, body parts and caste-specific morphologies are modified during postembryonic development under endocrine controls such as juvenile hormone (JH) and ecdysone. In addition to endocrine factors, developmental toolkit genes such as Hox- and appendage-patterning genes also contribute to the caste-specific body part modifications. These toolkits are thought to provide spatial information for specific morphogenesis. During social evolution, the complex crosstalks between physiological and developmental mechanisms should be established, leading to the sophisticated caste systems. This article reviews recent studies on these mechanisms underlying the termite caste differentiation and addresses implications for the evolution of caste systems in termites.
58Social interactions affecting caste development through physiological actions in termites.PubMed
Dai Watanabe, Hiroki Gotoh, Toru Miura, et al.
Front Physiol. 2014 Apr 9;5:127. doi: 10.3389/fphys.2014.00127. eCollection 2014.
A colony of social insects is not only an aggregation of individuals but also a functional unit. To achieve adaptive social behavior in fluctuating environmental conditions, in addition to coordination of physiological status in each individual, the whole colony is coordinated by interactions among colony members. The study on the regulation of social-insect colonies is termed "social physiology." Termites, a major group of social insects, exhibit many interesting phenomena related to social physiology, such as mechanisms of caste regulation in a colony. In their colonies, there are different types of individuals, i.e., castes, which show distinctive phenotypes specialized in specific colony tasks. Termite castes comprise reproductives, soldiers and workers, and the caste composition can be altered depending on circumstances. For the regulation of caste compositions, interactions among individuals, i.e., social interactions, are thought to be important. In this article, we review previous studies on the adaptive meanings and those on the proximate mechanisms of the caste regulation in termites, and try to understand those comprehensively in terms of social physiology. Firstly, we summarize classical studies on the social interactions. Secondly, previous studies on the pheromone substances that mediate the caste regulatory mechanisms are overviewed. Then, we discuss the roles of a physiological factor, juvenile hormone (JH) in the regulation of caste differentiation. Finally, we introduce the achievements of molecular studies on the animal sociality (i.e., sociogenomics) in terms of social physiology. By comparing the proximate mechanisms of social physiology in termites with those in hymenopterans, we try to get insights into the general principles of social physiology in social animals.
59High juvenile hormone titre and abdominal activation of JH signalling may induce reproduction of termite neotenics.PubMed
R Saiki, H Gotoh, K Toga, et al.
Insect Mol Biol. 2015 Aug;24(4):432-41. doi: 10.1111/imb.12169. Epub 2015 Apr 3.
Termite castes are a key example of polyphenism, in which reproductive division of labour is clearly seen in colonies. The reproductive castes in termites include primary and neotenic reproductives; primary reproductives found a new colony whereas neotenics succeed them in the reproductive role when the primary reproductives die or become senescent. Neotenics usually differentiate from nymphs or workers by developing functional gonads while retaining juvenile characteristics; however, the developmental mechanism during neotenic differentiation remains poorly understood. Juvenile hormone (JH) mediates a number of aspects of developmental regulation in caste differentiation in termites. In the present study we quantified JH titres in neotenic reproductives of Reticulitermes speratus, and compared these with other developmental stages. In addition, expression changes in JH signalling gene homologues (Methoprene-tolerant [Met], Krüppel-homolog1, Broad-Complex) in the head, thorax and abdomen were investigated during neotenic differentiation. Finally, we examined the function of Met in reproduction of neotenics by RNA interference (RNAi). Our results showed that the JH titres of neotenics were significantly higher than those of nymphs and workers. JH signalling genes were highly expressed in neotenic abdomens, compared with those in workers and nymphs. Met RNAi resulted in the inhibition of vitellogenin gene expression in newly moulted neotenics. These results suggest that the fertility of neotenics might be controlled by a large increase of JH titres and body-part-specific activation of JH signalling pathways.
60Hexamerin-based regulation of juvenile hormone-dependent gene expression underlies phenotypic plasticity in a social insect.PubMed
Xuguo Zhou, Matthew R Tarver, Michael E Scharf
Development. 2007 Feb;134(3):601-10. doi: 10.1242/dev.02755.
Worker termites of the genus Reticulitermes are temporally-arrested juvenile forms that can terminally differentiate into adultsoldier- or reproductive-caste phenotypes. Soldier-caste differentiation is a developmental transition that is induced by high juvenile hormone (JH) titers. Recently, a status quo hexamerin mechanism was identified, which reduces JH efficacy and maximizes colony fitness via the maintenance of high worker-caste proportions. Our goal in these studies was to investigate more thoroughly the influences of the hexamerins on JH-dependent gene expression in termite workers. Our approach involved RNA interference (RNAi), bioassays and quantification of gene expression. We first investigated the expression of 17 morphogenesis-associated genes in response to RNAi-based hexamerin silencing. Hexamerin silencing resulted in significant downstream impacts on 15 out of the 17 genes, suggesting that these genes are members of a JH-responsive genomic network. Next, we compared gene-expression profiles in workers after RNAi-based hexamerin silencing to that of (i) untreated workers that were held away from the colony; and (ii) workers that were also held away from the colony, but with ectopic JH. Here, although there was no correlation between hexamerin silencing and colony-release effects, we observed a significant correlation between hexamerin silencing and JH-treatment effects. These findings provide further evidence supporting the hypothesis that the hexamerins modulate JH availability, thus limiting the impacts of JH on termite caste polyphenism. Results are discussed in a context relative to outstanding questions on termite developmental biology, particularly on regulatory gene networks that respond to JH-, colony- and environmental-cues.
61Regulation of soldier caste differentiation by microRNAs in Formosan subterranean termite ( Shiraki).PubMed
He Du, Runmei Huang, Da-Song Chen, et al.
PeerJ. 2024 Feb 29;12:e16843. doi: 10.7717/peerj.16843. eCollection 2024.
The soldier caste is one of the most distinguished castes inside the termite colony. The mechanism of soldier caste differentiation has mainly been studied at the transcriptional level, but the function of microRNAs (miRNAs) in soldier caste differentiation is seldom studied. In this study, the workers of Shiraki were treated with methoprene, a juvenile hormone analog which can induce workers to transform into soldiers. The miRNomes of the methoprene-treated workers and the controls were sequenced. Then, the differentially expressed miRNAs (DEmiRs) were corrected with the differentially expressed genes DEGs to construct the DEmiR-DEG regulatory network. Afterwards, the DEmiR-regulated DEGs were subjected to GO enrichment and KEGG enrichment analysis. A total of 1,324 miRNAs were identified, among which 116 miRNAs were screened as DEmiRs between the methoprene-treated group and the control group. A total of 4,433 DEmiR-DEG pairs were obtained. No GO term was recognized as significant in the cellular component, molecular function, or biological process categories. The KEGG enrichment analysis of the DEmiR-regulated DEGs showed that the ribosome biogenesis in eukaryotes and circadian rhythm-fly pathways were enriched. This study demonstrates that DEmiRs and DEGs form a complex network regulating soldier caste differentiation in termites.
62Caste-specific microRNA expression in termites: insights into soldier differentiation.PubMed
M Matsunami, M Nozawa, R Suzuki, et al.
Insect Mol Biol. 2019 Feb;28(1):86-98. doi: 10.1111/imb.12530. Epub 2018 Oct 16.
Eusocial insects have polyphenic caste systems in which each caste exhibits characteristic morphology and behaviour. In insects, caste systems arose independently in different lineages, such as Isoptera and Hymenoptera. Although partial molecular mechanisms for the development of eusociality in termites have been clarified by the functional analysis of genes and hormones, the contribution of microRNAs (miRNAs) to caste differentiation is unknown. To understand the role of miRNAs in termite caste polyphenism, we performed small RNA sequencing in a subterranean termite (Reticulitermes speratus) and identified the miRNAs that were specifically expressed in the soldier and worker castes. Of the 550 miRNAs annotated in the R. speratus genome, 74 were conserved in insects and 174 were conserved in other termite species. We found that eight miRNAs (mir-1, mir-125, mir-133, mir-2765, mir-87a and three termite-specific miRNAs) are differentially expressed (DE) in soldiers and workers of R. speratus. This differential expression was experimentally verified for five miRNAs by real-time quantitative PCR. Further, four of the eight DE miRNAs in soldier and worker termite castes were also differentially expressed in hymenopteran castes. The finding that Isoptera and Hymenoptera shared several DE miRNAs amongst castes suggests that these miRNAs evolved independently in these phylogenetically distinct lineages.