Sexual signal loss, pleiotropy, and maintenance of a male reproductive polymorphism in crickets

Abstract

Pleiotropy between male signals and female preferences can facilitate evolution of sexual communication by maintaining coordi-nation between the sexes. Alternatively, it can favor variation in the mating system, such as a reproductive polymorphism. It is unknown how common either of these scenarios is in nature. In Pacific field crickets (Teleogryllus oceanicus) on Kauai, Hawaii, a mutation (flatwing) that segregates as a single locus is responsible for the rapid loss of song production in males. We used outbred cricket colonies fixed for male wing morph to investigate whether homozygous flatwing and normal-wing (wild-type) females differ in responsiveness to male calling song and propensity to mate when paired with either a flatwing or normal-wing male in the presence or absence of courtship song. Flatwing females were less likely to mount a male than normal-wing females. Females of both genotypes showed a preference for normal-wing males and were more likely to mate in the presence of courtship song; normal-wing females were particularly likely to mate with song. Our results show that negative pleiotropy between obligate male silence and female mating behavior can constrain the evolution of sexual signal loss and contribute to the maintenance of a male reproductive polymorphism in the wild. K E Y W O R D S : Female mating behavior, flatwing, genetic association, sexual signal evolution, sexual signal loss, Teleogryllus oceanicus.

Transregulation of an odorant binding protein by a proto-Y chromosome affects male courtship in house fly

“…Selection on Obp56h expression and male mating behavior could thus be weakened by trade-offs between mating behavior and stress response. This is consistent with the general prediction that pleiotropy can maintain genetic variance for sexually selected traits in natural populations (Kirkpatrick and Ryan 1991; Turelli and Barton 2004; Johnston et al 2013;Heinen-Kay et al 2020). Our results therefore provide a potential example of how the regulatory architecture underlying a sexually selected trait can create pleiotropic constraints that could impede selection on the trait, maintaining genetic variation in spite of strong selection on the trait.…”

Intralocus sexual conflict can maintain alternative reproductive tactics

“…There is nevertheless reason to think that intralocus sexual conflict could be a potent force that maintains variation in nature. Indeed, a growing body of evidence shows that selection on male ARTs and the traits that differentiate them results in correlated evolution in females: genetic linkage between male ARTs and female reproductive traits has been described in lizards (Sinervo and Zamudio 2001), crickets (Heinen-Kay et al 2020a; Richardson et al 2021), and bulb mites (Bielak et al 2014; Buzatto et al 2018; Buzatto and Clark 2020; Łukasiewicz et al 2020).…”

Sex‐specific associations between life‐history traits and a novel reproductive polymorphism in the Pacific field cricket

“…Our results bolster prior work showing that an important consequence of the evolution of a novel polymorphism in T. oceanicus is the correlations between the flatwing mutation and suites of other traits. For example, flatwing is linked with differences in cuticular hydrocarbons (Simmons et al., 2014), gene expression (Pascoal et al., 2016; Rayner et al., 2019), reproductive physiology (Bailey et al., 2010; Heinen‐Kay, Strub, et al., 2019), male reproductive success (Heinen‐Kay, Urquhart, et al., 2019) and female mating behaviour (Heinen‐Kay et al., 2020). The unique contribution of our results is to demonstrate that flatwing is also associated with differences in development time and body size.…”

“…Similarly, throat patch colour is associated with male mating strategy in the side‐blotched lizard ( Uta stansburiana ) with orange‐throated males defending large territories, blue‐throated males guarding single females and yellow‐throated males acting as nonterritorial ‘sneakers’ (Sinervo & Lively, 1996). Understanding how such polymorphisms arise and are maintained is an important focus of evolutionary biology as polymorphic systems provide critical insights into the processes underlying genetic and phenotypic diversity within species (Galeotti et al., 2003; Heinen‐Kay et al., 2020; McKinnon & Pierotti, 2010) and even the generation of new species (Hugall and Stuart Fox, 2012).…”

“…Although females do not express any wing traits associated with the mutation, being homozygous for the flatwing and normal‐wing alleles is associated with a host of effects in females. These include differences in gene expression (Pascoal et al., 2018; Rayner et al., 2019), reproductive investment and mating behaviour— flatwing homozygous females invest less in reproductive tissues (Heinen‐Kay et al., 2019) and show a lower propensity to mount males (Heinen‐Kay et al., 2020). This combination of advantageous and detrimental effects of the flatwing mutation in both males and females appears to contribute to the maintenance of the wing polymorphism.…”