Maintenance of Sperm Variation in a Highly Promiscuous Wild Bird

Sara Calhim,Andrew Cockburn,Tim R Birkhead,Michael C Double,Nicolas Margraf

doi:10.1371/journal.pone.0028809

Abstract

Postcopulatory sexual selection is an important force in the evolution of reproductive traits, including sperm morphology. In birds, sperm morphology is known to be highly heritable and largely condition-independent. Theory predicts, and recent comparative work corroborates, that strong selection in such traits reduces intraspecific phenotypic variation. Here we show that some variation can be maintained despite extreme promiscuity, as a result of opposing, copulation-role-specific selection forces. After controlling for known correlates of siring success in the superb fairy-wren (Malurus cyaneus), we found that (a) lifetime extra-pair paternity success was associated with sperm with a shorter flagellum and relatively large head, and (b) males whose sperm had a longer flagellum and a relatively smaller head achieved higher within-pair paternity. In this species extrapair copulations occur in the same morning, but preceding, pair copulations during a female's fertile period, suggesting that shorter and relatively larger-headed sperm are most successful in securing storage (defense), whereas the opposite phenotype might be better at outcompeting stored sperm (offense). Furthermore, since cuckolding ability is a major contributor to differential male reproductive output, stronger selection on defense sperm competition traits might explain the short sperm of malurids relative to other promiscuous passerines.

Highlights

Female promiscuity is a feature of the breeding system of most passerines, often leading to extrapair paternity (e.g. [1])
Males with sperm with a longer flagellum and relatively shorter heads were more successful at preventing cuckoldry (Fig. 2; binomial GLMMs with male identity as a random factor; flagellum length: estimate (6 s.e.) = 20.0868.31, z = 2.42, p = 0.016; flagellum:head ratio: estimate (6 s.e.) = 11.5064.31, z = 2.67, p = 0.008; n = 255 broods assigned to 47 males)
Our measure of cuckolding avoidance can be biased either way by future potential breeding attempts (n = 17 dominant males alive past the last available paternity analysis), removal of these data points did not change any of the previous results

Summary

Introduction

Female promiscuity is a feature of the breeding system of most passerines, often leading to extrapair paternity (e.g. [1]). Female promiscuity is a feature of the breeding system of most passerines, often leading to extrapair paternity Fitness in males that breed in social pairs but engage in extrapair copulations is the combined success of both extrapair and within-pair siring Several studies have looked at inter-male variation in a given trait and its concurrent and separate effect in within-pair and extrapair reproductive success in birds, yet these studies are largely limited to secondary sexual traits (i.e. plumage, song) or age (reviewed, n = 20 species). Focus on primary sexual traits and male copulation roles has largely been restricted to empirical studies of controlled matings in invertebrates [11]), hormonal manipulation in a wild passerine [12] and alternative mating tactics in centrarchid fish Focus on primary sexual traits and male copulation roles has largely been restricted to empirical studies of controlled matings in invertebrates (e.g. [8,9,10]), social status manipulation in domestic fowl (e.g. [11]), hormonal manipulation in a wild passerine [12] and alternative mating tactics in centrarchid fish (e.g. [13,14])

Methods

Results

Discussion

Conclusion