Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut.
Department of Integrative Biology, Institute for Neuroscience, The University of Texas at Austin, Austin, Texas.
Mol Ecol. 2019 Aug;28(15):3464-3481. doi: 10.1111/mec.14999. Epub 2019 Feb 6.
While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. "Nesting males" provide parental care, defend territories and form cooperative associations with unrelated "satellites," who cheat by sneaking fertilizations but help by reducing sperm competition from "sneakers" who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used "phenotypic engineering" that involved administering an androgen receptor antagonist (flutamide) to wild, free-living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down-regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite-directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.
虽然大量研究集中在社会互动如何演变，但很少有文献记录这些互动背后的神经内分泌机制对适应度的影响，尤其是在野外环境下。在这里，我们测量了雄性行为背后的神经内分泌机制如何影响斑鳍鱼（Symphodus ocellatus）的交配成功率和精子竞争。在这个物种中，雄性表现出三种不同的繁殖类型。“筑巢雄性”提供亲代养育，保卫领地，并与不相关的“卫星雄性”形成合作关系，后者通过偷偷受精来作弊，但通过减少不合作或不提供养育的“偷精者”的精子竞争来提供帮助。为了衡量这些社会互动背后的机制对适应度的影响，我们使用了“表型工程”，即给野生的、自由生活的鱼类施用雄激素受体拮抗剂（氟他胺）。用氟他胺处理的筑巢雄性将其攻击性从偷精者转移到卫星雄性身上，并且遭受偷精者的屈服性降低（这与筑巢雄性交配成功率降低有关）。控制雄性生殖行为的视前区（POA）在雄激素信号转导的实验操作后，雄激素受体（AR）和血管加压素 1a 受体（V1aR）mRNA 的表达显著下调。我们没有发现实验操作对雄性交配成功率、亲代身份或幼虫产量的直接影响。然而，实验操作引起的神经内分泌机制的变化与行为和交配成功率的变化显著相关：V1aR 表达与针对卫星雄性的攻击性呈负相关，其配体精氨酸血管加压素（AVT）的表达与求偶和交配成功率呈正相关，从而揭示了这些机制可能受到性选择的影响。
