“The consequences of polyandry for sibship structures, distributions of relationships and relatedness, and potential for inbreeding in a wild population”

Posted on

Ryan R. Germain, Peter Arcese, and Jane M. Reid (May 2018)

The DOI will be http://dx.doi.org/10.1086/696855

Female mating with multiple males reduces inbreeding potential among her offspring

A Song Sparrow (Melospiza melodia) resident on Mandarte Island, British Columbia, Canada.
(Credit: Ryan R. Germain)

In many species, females produce broods or litters of offspring with multiple fathers, but the actual benefits of this behavior (known as ‘polyandry’) remain largely unknown. One potential benefit could be that producing offspring with several males changes the degree to which a female’s descendants are related and could potentially mate with a relative (‘inbreed’) in the future. Because inbreeding can have severely negative consequences for any resulting offspring, theory predicts that the overall risk of inbreeding within a population should be lower when females produce offspring with multiple males. However, to date, no study has determined the actual effects of this process in wild populations with complex reproductive systems, such as females producing multiple broods or litters with the same or different males over their lifetimes, or where males themselves mate with multiple females.

In this study, researchers at the University of Aberdeen and the University of British Columbia used a long-term, island study population of Song Sparrows (Melospiza melodia) to determine the consequences of polyandry for inbreeding risk in future generations. Song sparrows form social pair-bonds where females and males cooperate to raise offspring, but DNA analysis reveals that about 28% of chicks in the population are fathered by a male other than their mother’s social mate. By comparing the actual genetic relatedness among all potential mates in the population with their relatedness had females only produced offspring with their social mate, this study finds that polyandry reduces the chances of inbreeding among close relatives (like full siblings) in future generations, but actually increases the chances of inbreeding among more distant relatives (like half-siblings). The overall conclusion of the study is that while polyandry can lead to some degree of reduced inbreeding in the future, thereby providing a benefit to this behavior, different aspects of mating systems in wild populations can substantially change this effect from what we would expect.


Abstract

The evolutionary benefits of simultaneous polyandry (female multiple mating within a single reproductive event) remain elusive. One potential benefit could arise if polyandry alters sibship structures and consequent relationships and relatedness among females’ descendants, and thereby intrinsically reduces future inbreeding risk (the ‘indirect inbreeding avoidance hypothesis’). However such effects have not been quantified in naturally complex mating systems that also encompass iteroparity, overlapping generations, sequential polyandry, and polygyny. We used long-term social and genetic pedigree data from song sparrows (Melospiza melodia) to quantify cross-generational consequences of simultaneous polyandry for offspring sibship structures and distributions of relationships and relatedness among possible mates. Simultaneous polyandry decreased full-sibships and increased half-sibships on average, but such effects varied among females and were smaller than would occur in the absence of sequential polyandry or polygyny. Further, while simultaneous polyandry decreased the overall frequencies of possible matings among adult full-sibs, it increased the frequencies of possible matings among adult half-sibs and more distant relatives. These results imply that the intrinsic consequences of simultaneous polyandry for inbreeding risk could cause weak indirect selection on polyandry, but the magnitude and direction of such effects will depend on complex interactions with other mating system components and the form of inbreeding depression.