Sexual selection on bushcricket genitalia operates in a mosaic pattern

Abstract

In most species with internal fertilization, male genitalia evolve faster than other morphological structures. This holds true for genital titillators, which are used exclusively during mating in several bushcricket subfamilies. Several theories have been proposed for the sexual selection forces driving the evolution of internal genitalia, especially sperm competition, sexually antagonistic coevolution (SAC), and cryptic female choice (CFC). However, it is unclear whether the evolution of genitalia can be described with a single hypothesis or a combination of them. The study of species‐specific genitalia action could contribute to the controversial debate about the underlying selective evolutionary forces. We studied female mating behaviors in response to experimentally modified titillators in a phylogenetically nested set of four bushcricket species: Roeseliana roeselii, Pholidoptera littoralis littoralis, Tettigonia viridissima (of the subfamily Tettigoniinae), and Letana inflata (Phaneropterinae). Bushcricket titillators have several potential functions; they stimulate females and suppress female resistance, ensure proper ampulla or spermatophore attachment, and facilitate male fixation. In R. roeselii, titillators stimulate females to accept copulations, supporting sexual selection by CFC. Conversely, titillator modification had no observable effect on the female's behavior in T. viridissima. The titillators of Ph. l. littoralis mechanically support the mating position and the spermatophore transfer, pointing to sexual selection by SAC. Mixed support was found in L. inflata, where manipulation resulted in increased female resistance (evidence for CFC) and mating failures by reduced spermatophore transfer success (evidence for SAC). Sexual selection is highly species‐specific with a mosaic support for either cryptic female choice or sexually antagonistic coevolution or a combination of both in the four species.

Evolution of male genitalia in the Drosophila repleta species group (Diptera: Drosophilidae)

“…As pointed out by several authors, in this complex structure that comprises the aedeagus, different sexual traits may simultaneously experience selection pressures from several evolutionary forces to varying degrees (e.g. Cordero & Eberhard, 2005; Kelly & Moore, 2016; McPeek et al., 2008; Wulff & Lehman, 2020). In this sense, the observed Brownian Motion pattern could be the outcome of random fluctuations of directional selection through deep time (Hansen & Martins, 1996) as a by‐product of processes of gradual deterministic evolution due to sexual selection and/or sexual conflict.…”

“…As pointed out by several authors, in this complex structure that comprises the aedeagus, different sexual traits may simultaneously experience selection pressures from several evolutionary forces to varying degrees (e.g. Cordero & Eberhard, 2005;Kelly & Moore, 2016;McPeek et al, 2008;Wulff & Lehman, 2020).…”

“…In the last decades, some consensus has been reached about male genital evolution as a phenomenon that happens very fast and is mainly driven by sexual selective processes (e.g. Arnqvist & Rowe, 2005; House et al., 2013; Dougherty & Shuker, 2016; Eberhard, 1990; Hagen et al., 2019; Hosken et al., 2019; Hosken & Stockley, 2004; House & Simmons, 2003; Simmons & Fitspatrick, 2019; Wulff & Lehman, 2020). On the other hand, the original idea that genital evolution is driven by species mate recognition using genital morphology to avoid hybridization, a hypothesis called lock‐and‐key (Dufour, 1844), has been strongly discredited (e.g.…”