Abstract

BackgroundExaggerated male ornaments and displays often evolve in species where males only provide females with ejaculates during reproduction. Although "good genes" arguments are typically invoked to explain this phenomenon, a simpler alternative is possible if variation in male reproductive quality (e.g. sperm number, ejaculate content, mating rate) is an important determinant of female reproductive success. The "phenotype-linked fertility hypothesis" states that female preference for male ornaments or displays has been selected to ensure higher levels of fertility and has driven the evolution of exaggerated male traits. Females of the stalk-eyed fly Teleopsis dalmanni must mate frequently to maintain high levels of fertility and prefer to mate with males exhibiting large eyespan, a condition-dependent sexual ornament. If eyespan indicates male reproductive quality, females could directly increase their reproductive success by mating with males with large eyespan. Here we investigate whether male eyespan indicates accessory gland and testis length, and then ask whether mating with large eyespan males affects female fertility.ResultsMale eyespan was a better predictor of two key male reproductive traits – accessory gland and testis length – than was body size alone. This positive relationship held true over three levels of increasing environmental stress during the maturation of the adult accessory glands and testes. Furthermore, females housed with a large eyespan male exhibited higher levels of fertility than those with small eyespan males.ConclusionMale eyespan in stalk-eyed flies is subject to strong directional mate preference and is a reliable indicator of male reproductive quality – both because males with larger eyespan have bigger accessory glands and testes, and also as they confer higher fertility on females. Fertility enhancement may have arisen because males with larger eyespan mated more often and/or because they transferred more sperm or other substances per ejaculate. The need to ensure high levels of fertility could thus have been an important selective force in the coevolution of female preference and male eyespan in stalk-eyed flies. Our results support the phenotype-linked fertility hypothesis and suggest that it might be of general importance in explaining the evolution of exaggerated male ornaments and displays in species where males only provide females with ejaculates during reproduction.

Highlights

  • Exaggerated male ornaments and displays often evolve in species where males only provide females with ejaculates during reproduction

  • We investigate whether male ornamentation signals reproductive quality in the stalk-eyed fly Teleopsis dalmanni, in particular, the ability of males to confer fertility

  • We examined whether male eyespan was positively correlated with the growth of the accessory glands and testes as a way of gauging variation in male reproductive quality

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Summary

Introduction

Exaggerated male ornaments and displays often evolve in species where males only provide females with ejaculates during reproduction. Females of the stalk-eyed fly Teleopsis dalmanni must mate frequently to maintain high levels of fertility and prefer to mate with males exhibiting large eyespan, a condition-dependent sexual ornament. Multiple copulations are required by females to achieve and maintain high fertility [5] This is probably because of the small size of the male spermatophore [6,7] and the small number of sperm stored following a single copulation (approximately 65 [8]). Meiotic drive impairs the development of Y-bearing sperm, causing lowered fertility in females mated to drive males [10,11]. Consistent with these findings, less than 40% of eggs laid by field-caught females failed to hatch, though the exact cause of this has yet to be established [12]

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