Macroevolutionary origin and adaptive function of a polymorphic female signal involved in sexual conflict

Inter-sexual signals that reveal developmental or mating status have evolved repeatedly in females of many animal lineages. Such signals can have important functions in sexual conflict over mating and can shape sexually antagonistic coevolution. However, we know little about how female signal development modifies mating harassment and thereby shape sexual conflict. Here, we combine phylogenetic comparative analyses of a color polymorphic damselfly genus (Ischnura) with behavioral experiments in one target species to investigate the evolutionary history and current adaptive function of female color development. Most Ischnura species have multiple female color morphs, one of which is typically male colored (“male mimics”). In our target species (I. elegans), males and male-mimicking females express a blue abdominal patch throughout post-emergence life. We demonstrate experimentally by phenotypic manipulations of this color signal, that in sexually dimorphic females, developmentally plastic expression of this signalling trait reduces pre-mating harassment prior to sexual maturity. Across species, this signal evolves rapidly, but in sexually dimorphic females, its origin is contingent upon the abdomen color expressed by co-occurring male-colored females. Our results suggest that cross-sexual transfer and subsequent co-option of an original male trait to a novel female anti-harassment function modulates sexual conflict driven by pre-mating interactions.

能够揭示发育状态或交配状态的性间信号，在众多动物类群的雌性个体中反复演化形成。这类信号在交配相关的性冲突中发挥重要作用，并可塑造性拮抗协同进化过程。然而，我们对雌性信号的发育如何调控交配骚扰，进而塑造性冲突的机制仍知之甚少。本研究通过对色彩多态蟌属（Ischnura）的系统发育比较分析，结合目标物种的行为实验，探究雌性色彩发育的演化历史与当前适应性功能。多数蟌属物种的雌性存在多种色彩型，其中一类通常呈现雄性体色，即雄性模仿型（male mimics）。在本研究的目标物种蓝尾蟌（I. elegans）中，雄性与雄性模仿型雌性在羽化后的整个生命周期中，腹部均带有蓝色斑块。本研究通过对该色彩信号的表型操控实验证实：在性二态雌性中，该信号性状的发育可塑性表达可降低性成熟前的交配前骚扰。跨物种分析显示，该信号演化速率较快，但在性二态雌性中，其起源取决于同域分布的雄性体色雌性所表达的腹部色彩。本研究结果表明，原始雄性性状的跨性别转移，以及后续将其招募为雌性全新的反骚扰功能，可调控由交配前互动介导的性冲突。