Strong functional integration among multiple parts of the complex male and female genitalia of stink bugs

Abstract

Genitalia are among the most studied phenotypes because they exhibit high anatomical diversity, experience fast evolutionary rates and may be shaped by several evolutionary mechanisms. A key element to uncover the mechanisms behind such impressive diversity is their copulatory function. This topic has been overlooked, especially concerning structures not directly involved in sperm transfer and reception. Here, we conduct a hypothesis-driven experimental study to elucidate the operation of various external genital parts in five species of stink bugs with differing levels of phylogenetic relatedness. These insects are unique because their male and female genitalia are externally well developed, rigid and composed of multiple components. In contrast with their anatomical complexity and diversity, we show that genital structures work jointly to perform a single function of mechanical stabilization during copula. However, distinct lineages have evolved alternative strategies to clasp different parts of the opposite sex. In spite of a high functional correspondence between male and female traits, the overall pattern of our data does not clearly support an intersexual coevolutionary scenario. We propose that the extraordinary male genital diversity in the family is probably a result of a process of natural selection enhancing morphological accommodation, but we consider alternative mechanisms.

Copulatory function and development shape modular architecture of genitalia differently in males and females

“…2017), we predict that (iii) male genitalia should be overall less integrated and more modular. Third, the general pattern of genital coupling among major groups of structures is conserved across pentatomids (Genevcius and Schwertner 2017), therefore, we also predict that (iv) the overall modular architecture of the genitalia has remained stable in evolutionary time, thus, modular patterns within species should match those among species.…”

“…We studied essentially all structures of the external, sclerotized male and female genitalia that have been shown to participate in the mechanical coupling of genitalia during mating (Genevcius and Schwertner 2017). Among these structures, we included 17 external genital parts that comprise four major structures in each genitalia (Table 1).…”

“…We highlight that we are only studying the external sclerotized genital parts, which are exclusively involved in the genital coupling. The internal, membranous genitalia have distinct functions like sperm transfer and storage (Wang and Millar 1997; Genevcius and Schwertner 2017), as well as distinct developmental origins (Tsai et al. 2011), making these structures a completely separate system.…”

“…Interestingly, a combination of these processes may operate simultaneously or sequentially on a single genital system (Rowe and Arnqvist 2012; Simmons 2014; Frazee and Masly 2015). This is possible because genital components usually have multiple functions (Wulff and Lehmann 2016; Genevcius and Schwertner 2017) and their development may be mediated by several genes and gene families (Dreyer and Shingleton 2019; Vincent et al. 2019).…”

“…We frame our study into a comparative approach addressing trait covariation at two different scales: among populations (within a single species) and in deep evolutionary time (among species in a tribe). For stink bugs, specific parts of the male genitalia interact with specific parts of females (Genevcius and Schwertner 2017), and these tight correspondences have been shown to determine correlated evolution (Genevcius et al. 2017).…”