Abstract
Inbreeding depression is commonly considered an evolutionary influence on pre-copulatory mechanisms of inbreeding avoidance. Inbreeding may be minimized by: (1) delayed maturation and reproduction, (2) sex-biased dispersal, (3) behavioural avoidance of mating with relatives, and/or (4) mating by females with multiple males (polyandry). Time constraints on reproduction and limited opportunities for outbred matings may limit mate choice, forcing females to mate with relatives and favouring multiple paternity to reduce the costs of inbred matings. Using parentage, relatedness, and spatial genetic analyses, we studied genetic mating system, dispersal and inbreeding patterns in a wild partially isolated colony of the yellow ground squirrels (Spermophilus fulvus), fast-living hibernators. Females were phylopatric, while males dispersed within the colony. Nevertheless, male-biased dispersal could not completely separate closely related males and females, and the potential risk of inbreeding was high, in particular due to early maturation of males — some of them matured before dispersal. Females did not mate assortatively with respect to relatedness of males, mating both with close kin and non-kin, and 38% of sire-mother pairs were closely related (coefficient of relatedness > 0.125). Multiple paternity was common (56% of all litters), and multiply sired litters combined offspring from inbred and outbred matings. Parents of singly sired litters were mostly unrelated. The overall level of inbreeding was low. We conclude that, under strong time constraints on reproduction and mate choice, females do not mate selectively with unrelated males. However, multiple paternity dilutes inbred matings effectively enough to maintain the overall low level of inbreeding.
Significance statement
Models predict that inbreeding should be more common in nature than is observed. Time constraints on reproduction and low availability of mates should make females tolerant of inbreeding, while multiple mating partners of females can help them reduce its costs. Based on observations in a free-living colony of the yellow ground squirrel, Spermophilus fulvus, a hibernator with a fast pace of life, we report high rates of inbred matings in females who have limited mate choice and face severe time constraints on reproduction. However, multiple paternity observed in more than half of females reduced the average relatedness between partners and, therefore, among their offspring, resulting in the overall low inbreeding within the colony. This is a new evidence for inbreeding tolerance under limited mate choice and female polyandry as a bet-hedging strategy against inbreeding.
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Data availability
The datasets generated and analysed during this study are available in the Figshare repository, https://doi.org/10.6084/m9.figshare.16574609
Code availability
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We thank V. Popov for the assistance in the field and B. Krasnov for the helpful comments on earlier versions and editing the text. We highly appreciate the constructive reviews and detailed suggestions for improving the manuscript by F. Stephen Dobson and one anonymous referee.
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The study was supported by grant from Russian Foundation for Basic Research (RFBR) to AVT (19–04-00577a).
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AVT conceived and supervised the study, LES, NAV, and AVT collected the data, ONB and SVT performed molecular genetic analyses, ONB, NAV, and AVT analysed the data and wrote the paper. All authors read and commented on the text and approved it.
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Batova, O.N., Vasilieva, N.A., Titov, S.V. et al. Female polyandry dilutes inbreeding in a solitary fast-living hibernator. Behav Ecol Sociobiol 75, 145 (2021). https://doi.org/10.1007/s00265-021-03086-1
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DOI: https://doi.org/10.1007/s00265-021-03086-1