Rapid differentiation and asynchronous coevolution of male and female genitalia in stink bugs

Abstract

Despite claims that genitalia are among the fastest evolving phenotypes, few studies have tested this trend in a quantitative and phylogenetic framework. In systems where male and female genitalia coevolve, there is a growing effort to explore qualitative patterns of evolution and their underlying mechanisms, but the temporal aspect remains overlooked. An intriguing question is how fast male and female genitalia may change in a coevolutionary scenario. Here, we apply a series of comparative phylogenetic analyses to reveal a scenario of correlated evolution and to investigate how fast male and female external, nonhomologous and functionally integrated genitalia change in a group of stink bugs. We report three findings: the female gonocoxite 8 and the male pygophore showed a clear pattern of correlated evolution, both genitalia were estimated to evolve much faster than nongenital traits, and rates of evolution of the male genitalia were twice as fast as the female genitalia. Our results corroborate the widely held view that male genitalia evolve fast and add to the scarce evidence for rapidly evolving female genitalia. Different rates of evolution exhibited by males and females suggest either distinct forms or strengths of selection, despite their tight functional integration and coevolution. The morphological characteristics of this coevolutionary trend are more consistent with a cooperative adjustment of the genitalia, suggesting a scenario of female choice, morphological accommodation, lock-and-key or some combination of the three.

Female genitalia are moderately informative for phylogenetic inference and not concerted with male genitalia in Saprininae beetles (Coleoptera: Histeridae)

“…The degree of homoplasy can be considered as a rough proxy for the character rate evolution, implying that a higher rate (more changes) corresponds to a higher degree of homoplasy (lower CI values). In this respect, we conclude that the female genitalia characters in Saprininae tend to evolve more slowly than other characters, which corroborates a similar finding in stink bugs (Genevcius et al ., ). Interestingly, the mean value of RI (index of grouping) in female genitalia (Table ) is higher than those in somatic and male genitalia characters, thus suggesting that female genitalia bear important phylogenetic signal to define certain clades despite having lower CI than other categories.…”

The evolution of genital shape variation in female cetaceans*

“…Even when male genital shape changes faster than female shape, female shape can be extremely variable (stink bugs; Genevcius et al. ). In cases where morphological variation in female genitalia are apparently subtle, careful quantification of shape variation has shown significantly different vaginal shapes despite some overlap in morphospace (watersnakes, Nerodia sipedon and N .…”

The evolution of female genitalia

“…In these taxa, the lengths of the female common and separate spermathecal ducts are highly divergent among 17 species, and the length of the common spermathecal duct has coevolved with the genital process of males (Kotrba et al, 2014). Several other studies have found similar patterns of female genital diversity and coevolutionary variation between female and male genitalia (Breed, Leigh, & Speight, 2013;Genevcius, Caetano, & Schwertner, 2017;Hedrick, Natanson, Brennan, Antalek-Schrag, & Conith, 2019;Horton & Lewis, 2011;Ilango & Lane, 2000;Ishikawa, 1987;Yoshizawa, Ferreira, Kamimura, & Lienhard, 2014).…”