Phylogenetic Mosaic of an Arms Race with Asymmetrical Sexual Conflict and Its Macroevolutionary Consequences in a Lineage of Small Water Striders

Abstract

Sexual conflict has been hypothesized as a driver of speciation, though its effects are likely heterogeneous across phylogenies and between sexes. The Gerromorpha (semi-aquatic bugs), which inhabits water surfaces across diverse aquatic environments, long served as a model for studying sexual conflict. While previous studies have focused on rapid antagonistic coevolution and the genetic basis of sexually antagonistic traits, the macroevolutionary consequences of asymmetrical sexual conflict-particularly male-dominated grasping traits versus female resistance-remain largely unexplored. Within the subgenus Pseudovelia, males exhibit pronounced phenotypic diversification in grasping structures, whereas females show modest, clade-specific resistance traits, suggesting male-biased asymmetric conflict. This system presents a valuable opportunity to examine how sexual conflict influences diversification and asymmetrical trait evolution across lineages. Using 204 individuals, representing over half of the subgenus's species diversity, we reconstructed a time-calibrated phylogeny, quantified diversification rates, assessed sexual conflict intensity across clades, and analyzed correlations between sexual trait evolution and diversification. Our results reveal extensive phylogenetic conflict, particularly within the East Asian clade, driven by introgression and incomplete lineage sorting (ILS). Furthermore, we observe significant phylogenetic heterogeneity in both phenotypic evolution and diversification rates. Notably, a male "trait package" enhancing grasping ability likely drives rapid diversification in the recently radiated "South China" lineage. In contrast, grasping traits involving abdominal segment VIII are associated with lower conflict intensity, facilitating greater evolutionary flexibility in female resistance and resulting in lineage-specific counter-adaptations. These findings highlight the heterogeneous dynamics of asymmetrical sexual conflict in shaping diversification and speciation.