Abstract

Dispersal in most group‐living species ensures gene flow among groups, but in cooperative social spiders, juvenile dispersal is suppressed and colonies are highly inbred. It has been suggested that such inbred sociality is advantageous in the short term, but likely to lead to extinction or reduced speciation rates in the long run. In this situation, very low levels of dispersal and gene flow among colonies may have unusually important impacts on fitness and persistence of social spiders. We investigated sex‐specific differences in dispersal and gene flow among colonies, as reflected in the genetic structure within colonies and populations of the African social spider Stegodyphus dumicola Pocock, 1898 (Eresidae). We used DNA fingerprinting and mtDNA sequence data along with spatial mapping of colonies to compare male and female patterns of relatedness within and among colonies at three study sites. Samples were collected during and shortly after the mating season to detect sex‐specific dispersal. Distribution of mtDNA haplotypes was consistent with proliferation of social nests by budding and medium‐ to long‐distance dispersal by ballooning females. Analysis of molecular variance and spatial autocorrelation analyses of AFLPs showed high levels of genetic similarity within colonies, and STRUCTURE analyses revealed that the number of source populations contributing to colonies ranged from one to three. We also showed significant evidence of male dispersal among colonies at one site. These results support the hypothesis that in social spiders, genetic cohesion among populations is maintained by long‐distance dispersal of female colony founders. Genetic diversity within colonies is maintained by colony initiation by multiple dispersing females, and adult male dispersal over short distances. Male dispersal may be particularly important in maintaining gene flow among colonies in local populations.

Highlights

  • Permanent group-living species run a risk of inbreeding, which could have detrimental fitness effects on offspring by increasing the likelihood of homozygosity of rare, lethal recessive alleles or more numerous weakly deleterious alleles (Charlesworth and Charlesworth 1987)

  • Using the fine-scale genetic data, we demonstrate how gene flow among colonies of a social spider may be maintained by sex-specific dispersal

  • Individuals in propagule nests shared the mtDNA haplotype of the nearest large nest; in two cases, the spiders in the propagule nests carried a different mtDNA from the nearest large nest: propagule 311b, located 6.6 m from colony 311, and propagule 349b, collected 12.3 m from colony 349

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Summary

Introduction

Permanent group-living (social) species run a risk of inbreeding, which could have detrimental fitness effects on offspring by increasing the likelihood of homozygosity of rare, lethal recessive alleles or more numerous weakly deleterious alleles (Charlesworth and Charlesworth 1987). Many social insect species have mating swarms or mating flights in which males and females from different colonies may meet and mate, for example, bumble bees Kin recognition and behavioral avoidance of mating among close relatives are known to occur in social species across the animal kingdom (Pusey and Wolf 1996).

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