Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Leclaire, Sarah; Nielsen, Johanna F.; Sharp, Stuart P.; Clutton‐Brock, Tim

doi:10.1111/jeb.12151

Cited by 29 publications

(31 citation statements)

References 70 publications

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“…; Kempenaers ; Szulkin & Sheldon ; Leclaire et al . ). However, the potential impact of non‐random pair formation and persistence on the degree to which polyandrous females could adjust offspring f through instantaneously random extra‐pair reproduction is not generally emphasized.…”

Section: Discussionmentioning

confidence: 97%

Demographic mechanisms of inbreeding adjustment through extra‐pair reproduction

Reid

Duthie

Wolak

et al. 2015

Journal of Animal Ecology

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One hypothesis explaining extra-pair reproduction is that socially monogamous females mate with extra-pair males to adjust the coefficient of inbreeding (f) of extra-pair offspring (EPO) relative to that of within-pair offspring (WPO) they would produce with their socially paired male. Such adjustment of offspring f requires non-random extra-pair reproduction with respect to relatedness, which is in turn often assumed to require some mechanism of explicit pre-copulatory or post-copulatory kin discrimination. We propose three demographic processes that could potentially cause mean f to differ between individual females’ EPO and WPO given random extra-pair reproduction with available males without necessarily requiring explicit kin discrimination. Specifically, such a difference could arise if social pairings formed non-randomly with respect to relatedness or persisted non-randomly with respect to relatedness, or if the distribution of relatedness between females and their sets of potential mates changed during the period through which social pairings persisted. We used comprehensive pedigree and pairing data from free-living song sparrows (Melospiza melodia) to quantify these three processes and hence investigate how individual females could adjust mean offspring f through instantaneously random extra-pair reproduction. Female song sparrows tended to form social pairings with unrelated or distantly related males slightly less frequently than expected given random pairing within the defined set of available males. Furthermore, social pairings between more closely related mates tended to be more likely to persist across years than social pairings between less closely related mates. However, these effects were small and the mean relatedness between females and their sets of potential extra-pair males did not change substantially across the years through which social pairings persisted. Our framework and analyses illustrate how demographic and social structuring within populations might allow females to adjust mean f of offspring through random extra-pair reproduction without necessarily requiring explicit kin discrimination, implying that adjustment of offspring f might be an inevitable consequence of extra-pair reproduction. New theoretical and empirical studies are required to explore the general magnitude of such effects and quantify the degree to which they could facilitate or constrain long-term evolution of extra-pair reproduction.

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Section: Discussionmentioning

confidence: 97%

Demographic mechanisms of inbreeding adjustment through extra‐pair reproduction

Reid

Duthie

Wolak

et al. 2015

Journal of Animal Ecology

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“…For example, Keller and Waller () review evidence for inbreeding depression in the wild (assumption 1); Leclaire et al. () and Arct et al. () review evidence across species for relatedness to the social mate increasing EPP (assumption 2); and Foerster et al.…”

mentioning

confidence: 99%

Inbreeding, inbreeding depression, and infidelity in a cooperatively breeding bird*

et al. 2018

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Inbreeding depression plays a major role in shaping mating systems: in particular, inbreeding avoidance is often proposed as a mechanism explaining extra‐pair reproduction in socially monogamous species. This suggestion relies on assumptions that are rarely comprehensively tested: that inbreeding depression is present, that higher kinship between social partners increases infidelity, and that infidelity reduces the frequency of inbreeding. Here, we test these assumptions using 26 years of data for a cooperatively breeding, socially monogamous bird with high female infidelity, the superb fairy‐wren (Malurus cyaneus). Although inbred individuals were rare (∼6% of offspring), we found evidence of inbreeding depression in nestling mass (but not in fledgling survival). Mother–son social pairings resulted in 100% infidelity, but kinship between a social pair did not otherwise predict female infidelity. Nevertheless, extra‐pair offspring were less likely to be inbred than within‐pair offspring. Finally, the social environment (the number of helpers in a group) did not affect offspring inbreeding coefficients or inbreeding depression levels. In conclusion, despite some agreement with the assumptions that are necessary for inbreeding avoidance to drive infidelity, the apparent scarcity of inbreeding events and the observed levels of inbreeding depression seem insufficient to explain the ubiquitous infidelity in this system, beyond the mother–son mating avoidance.

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“…In addition to the assumptions that EPO should have a reduced degree of inbreeding and that there is inbreeding depression in the population, the inbreeding avoidance hypothesis also predicts that more closely related pairs should have higher EPP rates (Leclaire et al. ; Arct et al. ).…”

mentioning

confidence: 99%

Indirect fitness benefits through extra‐pair mating are large for an inbred minority, but cannot explain widespread infidelity among red‐winged fairy‐wrens

et al. 2019

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Extra‐pair paternity (EPP) has been suggested to improve the genetic quality of offspring, but evidence has been equivocal. Benefits of EPP may be only available to specific individuals or under certain conditions. Red‐winged fairy‐wrens have extremely high levels of EPP, suggesting fitness benefits might be large and available to most individuals. Furthermore, extreme philopatry commonly leads to incestuous social pairings, so inbreeding avoidance may be an important selection pressure. Here, we quantified the fitness benefits of EPP under varying conditions and across life‐stages. Extra‐pair offspring (EPO) did not appear to have higher fitness than within‐pair offspring (WPO), neither in poor years nor in the absence of helpers‐at‐the‐nest. However, EPP was beneficial for closely related social pairs, because inbred WPO suffered an overall 75% reduction in fitness. Inbreeding depression was nonlinear and reduced nestling body condition, first year survival and reproductive success. Our comprehensive study indicates that EPP should be favored for the 17% of females paired incestuously, but cannot explain the widespread infidelity in this species. Furthermore, our finding that fitness benefits of EPP only become apparent for a small part of the population could potentially explain the apparent absence of fitness differences in population wide comparisons of EPO and WPO.

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Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Cited by 29 publications

References 70 publications

Demographic mechanisms of inbreeding adjustment through extra‐pair reproduction

Demographic mechanisms of inbreeding adjustment through extra‐pair reproduction

Inbreeding, inbreeding depression, and infidelity in a cooperatively breeding bird*

Indirect fitness benefits through extra‐pair mating are large for an inbred minority, but cannot explain widespread infidelity among red‐winged fairy‐wrens

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