Pre‐ and Post‐Copulatory Sexual Traits Influence Male Fitness Across a Mosaic Hybrid Zone

TL;DR

This study shows how pre- and post-copulatory traits affect male reproductive success in hybridizing sparrow species, influencing gene flow and hybridization patterns.

Contribution

The study identifies context-dependent drivers of male fitness and sexual selection in a hybrid zone, revealing how these factors influence asymmetric introgression.

Findings

Saltmarsh sparrows had higher reproductive output and greater variance in reproductive success compared to Nelson's and hybrid males.

Body size was the best predictor of reproductive success, indicating pre-copulatory sexual selection.

Post-copulatory traits like cloacal protuberance volume and sperm length correlated with the number of offspring sired, showing sperm competition.

Abstract

Primary and secondary male sexual traits can influence the interspecific interactions of hybridizing populations, yielding fitness consequences and either promoting or restricting gene flow. In this study, we evaluated the relative male fitness of two species of hybridizing tidal marsh endemics: saltmarsh (
Ammospiza caudacutus
) and Nelson's sparrows (
A. nelsoni
) and assessed the effects of male condition and competitive ability on resulting patterns of paternity and gene flow. We compared reproductive success (number of offspring sired) among saltmarsh, Nelson's, and hybrid sparrow males (n = 125) and modeled male fitness in relation to measured pre‐copulatory (body size, fat scores, and muscle scores) and post‐copulatory (cloacal protuberance (CP) volume and sperm length) male sexual traits across two sites within the center of the hybrid zone. We found saltmarsh sparrows had higher levels of skew in fertilization success than Nelson's and greater reproductive output than both Nelson's and hybrids, suggesting interspecific competition may occur. Body size was the best predictor of reproductive success, independent of male genotypes, providing evidence for a role of pre‐copulatory sexual selection. We also found evidence of post‐copulatory sexual selection and sperm competition contributing to patterns of hybridization, with CP volume and sperm length increasing with number of offspring sired. Differential mean fitness by species may influence patterns of hybridization and has the potential to drive asymmetrical introgression; however, the drivers of male fitness differed between species and sites, suggesting the level of sexual selection and resulting patterns of gene flow are context dependent and not stable across a small sptatial scale within the center of this mosaic hybrid zone. Overall, few interspecific offspring and nearly equal backcrossing in both parental species within the center of the hybrid zone suggest mechanisms such as reinforcement exist to limit hybridization and minimize asymmetric introgression.

We used SNP genotypes to assess and compare male reproductive success in two inter‐breeding species of marsh sparrow—saltmarsh and Nelson's sparrow—and their hybrids. Saltmarsh sparrow males had higher reproductive output, greater variance in reproductive success, and higher levels of multiple paternity than Nelson's sparrows and hybrids. We found evidence for both pre‐copulatory (body size) and post‐copulatory (sperm competition) sexual selection, with drivers of fitness differing between the two species. Photo shows a pair of mating saltmarsh sparrows (credit: Grace McCulloch).

Figures