Have Male and Female Genitalia Coevolved? A Phylogenetic Analysis of Genitalic Morphology and Sexual Size Dimorphism in Web-Building Spiders (Araneae: Araneoidea)

Abstract

Abstract.•Sexual size dimorphism (SSD) can strongly influence the evolution of reproductive strategies and life history. If SSD is extreme, and other characters (e.g., genitalic size) also increase with size, then functional conflicts may arise between the sexes. Spiders offer an excellent opportunity to investigate this issue because of their wide range of SSD. By using modern phylogenetic methods with 16 species of orb-weaving spiders, we provide strong evidence for the "positive genitalic divergence" model, implying that sexual genitalic dimorphism (SGD) increases as SSD increases. This pattern is supported by an evolutionary mismatch between the absolute sizes of male and female genitalia across species. Indeed, our findings reveal a dramatic reversal from male genitalia that are up to 87X larger than female genitalia in size-monomorphic species to female genitalia that are up to 2.8 X larger in extremely size-dimorphic species. We infer that divergence in SGD could limit SSD both in spiders, and potentially in other taxa as well. Further, male and female body size, as well as male and female genitalia size, are decoupled evolutionarily. Finally, we show a negative scaling (hypoallometry) of male and female genitalic morphology within sexes. Evolutionary forces specific to each sex, such as larger female size (increased fecundity) or smaller male size (enhanced mate-searching ability), may be balanced by stabilizing selection on relative genitalic size.

One size fits all? Determinants of sperm transfer in a highly dimorphic orb‐web spider

“…Interestingly, spermatheca size correlates positively with the number of sperm transferred, potentially limiting male transfer success. This is in contradiction to previous comparative analyses which suggested that females in dimorphic species have such large spermathecae to encourage multiple mating (Ramos et al ., ). Below we discuss these results in detail.…”

“…Thus, no particular scaling relationship between spermathecae size and body size is predicted by any of the currently debated sexual conflict/sexual selection hypotheses for the evolution of genitalic traits. A hypo‐allometric relationship between body size and spermatheca size has been found based on cross‐species comparisons (Ramos et al ., ) and could be the result of a common genetic background, shared with the other genitalic traits (‘genetic constraints’). However, because females are so much bigger than males in highly dimorphic species, genital dimorphism changes from male‐biased in monomorphic species to female‐biased in species with extreme SSD.…”

Mechanisms and Evidence of Genital Coevolution: The Roles of Natural Selection, Mate Choice, and Sexual Conflict

“…Second, when size dimorphism is marked, selection can operate to match genital size. In orbweaving spiders with extreme size dimorphism, tiny males have disproportionally large genitalia (up to 20% of their body mass) to match female genital size (Ramos et al 2005). This has not been examined when males are larger than fe-males, but females may be predicted to enlarge their genitalia to accommodate large male genitalia (Langerhans 2011).…”

Evolution of the male genitalia: morphological variation of the aedeagi in a natural population of Drosophila mediopunctata

“…Due to these, we concluded that among the three major hypotheses, the lock-and-key hypothesis can not be supported by our data, but the other two-pleiotropy and sexual selection-can not be ruled out. However, other studies are needed to further understand animal genitalia evolution such as: the female genitalia (Ramos et al 2005); measurements of successful evolution of the male genitalia (using, for example, total offspring); tests of female preference regarding aedeagus size and shape; and tests for male vigor depending on aedeagus morphology.…”