Obligately silent males sire more offspring than singers in a rapidly evolving cricket population

Abstract

How sexual traits are gained and lost in the wild remains an important question in evolutionary biology. Pacific field crickets ( Teleogryllus oceanicus ) in Hawaii provide an unprecedented opportunity to investigate the factors facilitating evolutionary loss of a sexual signal in real time. Natural selection from an acoustically orienting parasitoid fly drove rapid evolution of a novel, silent male morph. While silent (flatwing) males enjoy protection from the fly, they face difficulty attracting mates. We tested how offspring production varies in association with three male attributes affected by the spread of flatwing: wing morph (flatwing or normal-wing), age (flatwings should survive longer than singers) and exposure to calling song during rearing (wild populations with many flatwings lack ambient calling song). Per mating event, flatwings sired more offspring than singers and older males were mounted more quickly by females when presented with standard courtship song. Despite prior work showing that male age and acoustic experience influence sperm characteristics associated with fertilization, age and song exposure had no influence on male offspring production per mating. This represents the first evidence that the silent male morph possesses a reproductive advantage that may help compensate for precopulatory barriers to mate attraction.

Direct and indirect effects of sexual signal loss on female reproduction in the Pacific field cricket (Teleogryllus oceanicus)

“…Kauai males show a similar pattern of reproductive tissue investment associated with the wing mutation, where normal‐wing males possess heavier testes than flatwing males (Bailey et al., ; Rayner et al., ). Kauai males also exhibit an inconsistency between potential and actual reproductive outcomes, as flatwing males sire more offspring than normal‐wings when mated to a normal‐wing female (Heinen‐Kay et al., ). At present, the mechanism underlying this discrepancy is unclear in both males and females.…”

“…Social exposure to sexual signals is also known to influence reproductive physiology in male crickets. Male T. oceanicus raised in the absence of calling song, mimicking a population with high density of flatwing males or few competitors, invested less in testes size (Bailey et al., ) and exhibit lower sperm viability (Gray & Simmons, ), although acoustic experience does not appear to affect male reproductive success (Heinen‐Kay et al., ). Most studies have found that female crickets reared in the absence of song show reduced investment in reproductive tissues (Bateman, Verburgt, & Ferguson, ; Conroy & Roff, ; Kasumovic, Chen, & Wilkins, ; Kasumovic, Hall, Try, & Brooks, ; Rebar, Barbosa, & Greenfield, ), similar to males, while one study showed no effect of acoustic experience on egg laying (Lierheimer & Tinghitella, ).…”

“…Briefly, males can act as a satellite to a calling male and intercept females responding to the caller's song. Flatwing males experience other pleiotropic effects of the mutation, including differences in gene expression (Pascoal et al, 2014(Pascoal et al, , 2016, cuticular hydrocarbons (Simmons et al, 2014), and reproductive physiology -flatwing males have smaller testes (Bailey et al, 2010;Rayner et al, 2019) but benefit by siring more offspring per mating event than normal-wings (Heinen-Kay, Urquhart, & Zuk, 2019). Females can be homozygous or heterozygous carriers of flatwing but show no obvious morphological indication of their genotype.…”

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

“…Flatwing males also possess a reproductive advantage and sire more offspring than normal‐wings per successful mating event (Heinen‐Kay et al. 2019b). However, silent males face major precopulatory barriers to mating because they cannot sing, and normal‐wing males are favored by sexual selection (Tanner et al.…”

“…Studies that have decoupled courtship song from male wing morph show that females are less likely to mate in the absence of courtship song, and do not discriminate between males based solely on their wing morph (Heinen‐Kay et al. 2019b; Kota et al. unpubl.…”