Abstract

Sex-biased dispersal is pervasive and has diverse evolutionary implications, but the fundamental drivers of dispersal sex biases remain unresolved. This is due in part to limited diversity within taxonomic groups in the direction of dispersal sex biases, which leaves hypothesis testing critically dependent upon identifying rare reversals of taxonomic norms. Here, we use a combination of observational and genetic data to demonstrate a rare reversal of the avian sex bias in dispersal in the cooperatively breeding white-browed sparrow weaver (Plocepasser mahali). Direct observations revealed that (i) natal philopatry was rare, with both sexes typically dispersing locally to breed, and (ii), unusually for birds, males bred at significantly greater distances from their natal group than females. Population genetic analyses confirmed these patterns, as (i) corrected Assignment index (AIc), FST tests and isolation-by-distance metrics were all indicative of longer dispersal distances among males than females, and (ii) spatial autocorrelation analysis indicated stronger within-group genetic structure among females than males. Examining the spatial scale of extra-group mating highlighted that the resulting ‘sperm dispersal’ could have acted in concert with individual dispersal to generate these genetic patterns, but gamete dispersal alone cannot account entirely for the sex differences in genetic structure observed. That leading hypotheses for the evolution of dispersal sex biases cannot readily account for these sex-reversed patterns of dispersal in white-browed sparrow weavers highlights the continued need for attention to alternative explanations for this enigmatic phenomenon. We highlight the potential importance of sex differences in the distances over which dispersal opportunities can be detected.

Highlights

  • Dispersal is a fundamental process in ecology that has a profound influence at multiple levels of organization, from the reproductive success of individuals to the genetic structure and viability of populations

  • The most robust estimates of sex differences in dispersal can be derived using a combination of direct observational data and indirect population genetic methods (e.g. Ribeiro et al 2012; Rollins et al 2012), integrating where possible information on spatial patterns of extra-pair mating to account for gamete dispersal (e.g. Double et al 2005; see Smouse & Peakall 1999; Vekemans & Hardy 2004 for gamete dispersal in plants)

  • Dominant breeding positions were rarely inherited by birds within their natal groups (8 of 54 dominance turnover events, 14.8%), and there was no clear sex difference in the incidence of doing so (3 of 25 (12.0%) female dominance turnovers; 5 of 29 males (17.2%); binomial test: v21 = 0.03, P = 0.88)

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Summary

Introduction

Dispersal is a fundamental process in ecology that has a profound influence at multiple levels of organization, from the reproductive success of individuals to the genetic structure and viability of populations. Previous studies have demonstrated that estimates based on genetic data alone can differ from estimates derived from observational data (Winters & Waser 2003; Lukas et al 2005; Harris et al 2009; Rollins et al 2012) Such differences may arise in part because indirect genetic methods examine the population genetic patterns arising from both the permanent dispersal of individuals and the spread of gametes (e.g. in species that temporarily move to mate; Waser & Elliott 1991; Double et al 2005; Griesser et al 2013), and in some cases, the genetic signature of gamete dispersal can shroud or exaggerate that of individual dispersal (Winters & Waser 2003). The most robust estimates of sex differences in dispersal can be derived using a combination of direct observational data and indirect population genetic methods (e.g. Ribeiro et al 2012; Rollins et al 2012), integrating where possible information on spatial patterns of extra-pair mating to account for gamete dispersal (e.g. Double et al 2005; see Smouse & Peakall 1999; Vekemans & Hardy 2004 for gamete dispersal in plants)

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