Abstract
Post-copulatory interactions between males and females involve highly coordinated, complex traits that are often rapidly evolving and divergent between species. Failure to produce and deposit eggs may be a common post-mating prezygotic barrier, yet little is known about what prevents the induction of egg-laying between species. The field crickets, Gryllus firmus and G. pennsylvanicus are isolated by a one-way reproductive incompatibility; G. pennsylvanicus males fail to fertilize G. firmus eggs or to induce normal egg-laying in G. firmus females. We use experimental crosses to elucidate the role of accessory gland-derived vs. testis-derived components of the G. firmus male ejaculate on egg-laying in conspecific and heterospecific crosses. Using surgical castrations to create ‘spermless’ males that transfer only seminal fluid proteins (SFPs) we test whether G. firmus male SFPs can induce egg-laying in conspecific crosses and rescue egg-laying in crosses between G. pennsylvanicus males and G. firmus females. We find G. firmus SFPs induce only a small short-term egg-laying response and that SFPs alone cannot explain the normal induction of egg-laying. Gryllus firmus SFPs also do not rescue the heterospecific cross. Testis-derived components, such as sperm or prostaglandins, most likely stimulate egg-laying or act as transporters for SFPs to targets in the female reproductive tract. These results highlight the utility of experimental approaches for investigating the phenotypes that act as barriers between species and suggest that future work on the molecular basis of the one-way incompatibility between G. firmus and G. pennsylvanicus should focus on divergent testis-derived compounds or proteins in addition to SFPs.
Highlights
Traits that mediate interactions between males and females are critical for reproduction and yet often evolve rapidly and are highly divergent between species
The egg-count data were highly overdispersed; we modeled the total number of eggs laid by G. firmus females after 48 h using generalized linear mixed model (GLMM) with a Poisson distribution, individual-level random effects [42], and male treatment as the predictor
The nature of the one-way incompatibility between G. firmus females and G. pennsylvanicus males suggests a role for seminal fluid proteins (SFPs), and both egg-laying and fertilization are traits that are often mediated by SFPs in other taxa
Summary
Traits that mediate interactions between males and females are critical for reproduction and yet often evolve rapidly and are highly divergent between species. Egg-laying is a multi-step process that involves egg production within the ovary (oogenesis), release of the egg from ovary into the oviducts (ovulation), progression of the egg down the oviducts, union of the sperm and egg within the genital chamber (fertilization) and the deposition of the egg into a particular substrate (oviposition). These steps are tightly linked to the proper transfer and storage of the male ejaculate. A reduction in the efficiency or a failure at any of these steps can lead to reproductive incompatibilities in insects
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