Spermatophore retention may accommodate sexual signal loss in Pacific field crickets

Abstract: Sexual signals are gained and lost over evolutionary time. While signal gain has obvious fitness benefits, signal loss should present significant costs due to decreased mating opportunities. Just as female mating preferences can promote evolutionary gain and elaboration of sexual signals, they may also maintain signal loss. We investigated how two components of female mate choice are involved in rapid sexual signal loss in the Pacific field cricket (Teleogryllus oceanicus), in which many males have lost the ability to sing. Males that can sing (“normal-wings”) and obligately silent males (“flatwings”) coexist in Hawaiian populations. While we know that females prefer not to mate with flatwings, we tested whether females discriminate against flatwing males before copulation due to the lack of a song or something inherent about their wing morphology. We combined this assessment with a test of post-copulatory preference by presenting females with either a normal-wing or flatwing male in the presence or absence of a courtship song stimulus. Females took significantly longer to mount males in the absence of a courtship song regardless of male wing morph. This is the first evidence that females discriminate against the absence of a song during mate choice, not male wing morph. However, females retained spermatophores for equally long regardless of male wing morph and whether they heard a courtship song, suggesting no post-copulatory barriers in the absence of a song. Pre- and post-copulatory sexual selections may not operate synchronously in this system, which may help explain the success of the silent morph in wild populations. Significance statement: Signal loss is ubiquitous in nature, despite the associated decrease in mating opportunities. We assessed how the interaction of pre- and post-copulatory preferences may accommodate signal loss. Song attracts mates in Pacific field crickets, but some males have lost the ability to sing in response to an acoustically orienting parasitoid. We measured how long females took to mount males (pre-copulatory choice) and the length of sperm transfer, i.e., spermatophore retention time (post-copulatory choice), when presented with normal and silent males in the presence and absence of a song stimulus. Females took longer to mate in the absence of a courtship song but kept spermatophores for full sperm transfer, regardless of song presence or male type. Pre-copulatory choice in this system acts against silent males, while post-copulatory choice may not. Asynchrony between these two episodes of sexual selection may allow signal loss to persist in spite of the challenges it presents to mating.