Data from: Fluctuating selection strength and intense male competition underlie variation and exaggeration of a water strider’s male weapon

Sexually selected traits can reach high degrees of expression and variation under directional selection. A growing number of studies suggest that such selection can vary in space, time and form within and between populations. However, the impact of these fluctuations on sexual trait expression is poorly understood. The water strider Microvelia longipes displays a striking case of exaggeration and phenotypic variation where males display extreme differences in the size of their rear legs. To study the origin and maintenance of this exaggerated trait, we conducted comparative behavioral and morphometric experiments in a sample of Microvelia species. We uncovered differences both in the mating behavior and the degree of sexual dimorphism across these species. Interestingly, M. longipes evolved a specific mating behavior where males compete for egg-laying sites, consisting of small floating objects, to intercept and copulate with gravid females. Through male-male competition assays, we demonstrated that male rear legs are used as weapons to dominate egg-laying sites and that intense competition is associated with the evolution of rear leg length exaggeration. Field observations revealed rapid fluctuation in M. longipes habitat stability and the abundance of egg-laying sites. Paternity tests using genetic markers demonstrated that small males could only fertilize about 5% of the eggs when egg-laying sites are limiting, whereas this proportion increased to about 20% when egg-laying sites become abundant. Furthermore, diet manipulation and artificial selection experiments also showed that the exaggerated leg length in M. longipes males is influenced by both genetic and nutritional factors. Collectively, our results highlight how fluctuation in the strength of directional sexual selection, through changes in the intensity of male competition, can drive the exaggeration and phenotypic variation in this weapon trait.

性选择性状在定向选择作用下可呈现极高的表达程度与表型变异水平。越来越多的研究表明，这类选择在种群内部及种群间可随空间、时间及作用形式发生变化。然而，此类波动对性选择性状表达的影响仍未得到充分阐释。水黾科微黾属的长角微黾（Microvelia longipes）呈现出一例极具代表性的性状夸张与表型变异案例：其雄性个体的后足尺寸存在极端差异。为探究该夸张性状的起源与维持机制，我们以多个微黾属物种为研究对象，开展了比较行为学与形态计量学实验。研究发现，这些物种在交配行为与性二态性程度上均存在差异。值得注意的是，长角微黾演化出了一种独特的交配行为：雄性会争夺由小型漂浮物构成的产卵位点，以此拦截并与受孕雌性交配。通过雄性间竞争实验，我们证实雄性后足可作为武器以争夺产卵位点，且激烈的雄性竞争与后足长度夸张性状的演化密切相关。野外观测表明，长角微黾的生境稳定性与产卵位点丰度会发生快速波动。利用遗传标记进行的父权分析显示，当产卵位点有限时，体型较小的雄性仅能使约5%的卵完成受精；而当产卵位点充足时，这一比例可提升至约20%。此外，饮食操控与人工选择实验亦表明，长角微黾雄性夸张的后足长度同时受遗传与营养因素调控。综合来看，本研究结果揭示了定向性选择强度的波动如何通过改变雄性竞争强度，进而推动该武器性状的夸张化演化与表型变异。