Abstract

Inbreeding is widely hypothesized to shape mating systems and population persistence, but such effects will depend on which traits show inbreeding depression. Population and evolutionary consequences could be substantial if inbreeding decreases sperm performance and hence decreases male fertilization success and female fertility. However, the magnitude of inbreeding depression in sperm performance traits has rarely been estimated in wild populations experiencing natural variation in inbreeding. Further, the hypothesis that inbreeding could increase within‐ejaculate variation in sperm traits and thereby further affect male fertilization success has not been explicitly tested. We used a wild pedigreed song sparrow (Melospiza melodia) population, where frequent extrapair copulations likely create strong postcopulatory competition for fertilization success, to quantify effects of male coefficient of inbreeding (f) on key sperm performance traits. We found no evidence of inbreeding depression in sperm motility, longevity, or velocity, and the within‐ejaculate variance in sperm velocity did not increase with male f. Contrary to inferences from highly inbred captive and experimental populations, our results imply that moderate inbreeding will not necessarily constrain sperm performance in wild populations. Consequently, the widely observed individual‐level and population‐level inbreeding depression in male and female fitness may not stem from reduced sperm performance in inbred males.

Highlights

  • Inbreeding and consequent inbreeding depression, defined as reduced mean fitness in offspring resulting from mating between relatives, is widely hypothesized to drive the evolution of mating systems and mate choice (Charlesworth, 2006; Szulkin, Stopher, Pemberton, & Reid, 2013; Tregenza & Wedell, 2000) and to increase population extinction risk (Crnokrak & Roff, 1999; Hedrick & Kalinowski, 2000; Kenney, Allendorf, McDougal, & Smith, 2014)

  • The magnitude of inbreeding depression in sperm performance traits has rarely been estimated in wild populations experiencing natural variation in inbreeding

  • We found no evidence of inbreeding depression in sperm motility, longevity, or velocity, and the within-­ejaculate variance in sperm velocity did not increase with male f

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Summary

| INTRODUCTION

Inbreeding and consequent inbreeding depression, defined as reduced mean fitness in offspring resulting from mating between relatives, is widely hypothesized to drive the evolution of mating systems and mate choice (Charlesworth, 2006; Szulkin, Stopher, Pemberton, & Reid, 2013; Tregenza & Wedell, 2000) and to increase population extinction risk (Crnokrak & Roff, 1999; Hedrick & Kalinowski, 2000; Kenney, Allendorf, McDougal, & Smith, 2014). Under risk of sperm competition, males might trade-­off resources between traits that reduce sperm competition (e.g., increased mate guarding) versus traits that increase fertilization success (e.g., increased sperm quality, Kelly & Jennions, 2011; Schradin, Eder, & Müller, 2012) Such status-­ dependent investment, where non-­mate-­guarding floater, satellite, or sneaker males exhibit better sperm performance than dominant mate-­ guarding males, has been observed in captive and wild vertebrates (Fasel et al, 2016; Fitzpatrick, Desjardins, Milligan, Montgomerie, & Balshine, 2007; Froman, Pizzari, Feltmann, Castillo-­Juarez, & Birkhead, 2002; Neff, Fu, & Gross, 2003; Stockley, Searle, Macdonald, & Jones, 1994). We tested whether the mean and variance in these traits differed between socially paired and socially unpaired males, which have different opportunities for mate guarding and might experience different trade-­offs regarding sperm performance

| MATERIAL AND METHODS
Findings
| DISCUSSION
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