Promiscuous mating produces offspring with higher lifetime fitness

Gerlach, Nicole; McGlothlin, Joel W.; Parker, Patricia G.; Ketterson, Ellen D.

doi:10.1098/rspb.2011.1547

Cited by 46 publications

(53 citation statements)

References 52 publications

(75 reference statements)

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“…Predator mobbing is common in tree swallows ( Tachycineta bicolor ), and here older and experienced females had more extra-pair sires [102], higher hatching success [103], and larger clutch size [104]. In dark-eyed juncos ( Junco hyemalis ) extra-pair offspring had higher fitness: sons through extra-pair offspring and daughters through increased fecundity [100], which is as expected from our theory if female extra-pair mating and male cooperative investment are heritable traits. It would be interesting to see further analyses of whole-nest and neighbourhood effects and to contrast populations of the same species differing in the level of extra-pair paternity.…”

Section: Discussionsupporting

confidence: 81%

Extra-Pair Mating and Evolution of Cooperative Neighbourhoods

Eliassen

Jørgensen

2014

PLoS ONE

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A striking but unexplained pattern in biology is the promiscuous mating behaviour in socially monogamous species. Although females commonly solicit extra-pair copulations, the adaptive reason has remained elusive. We use evolutionary modelling of breeding ecology to show that females benefit because extra-pair paternity incentivizes males to shift focus from a single brood towards the entire neighbourhood, as they are likely to have offspring there. Male-male cooperation towards public goods and dear enemy effects of reduced territorial aggression evolve from selfish interests, and lead to safer and more productive neighbourhoods. The mechanism provides adaptive explanations for the common empirical observations that females engage in extra-pair copulations, that neighbours dominate as extra-pair sires, and that extra-pair mating correlates with predation mortality and breeding density. The models predict cooperative behaviours at breeding sites where males cooperate more towards public goods than females. Where maternity certainty makes females care for offspring at home, paternity uncertainty and a potential for offspring in several broods make males invest in communal benefits and public goods. The models further predict that benefits of extra-pair mating affect whole nests or neighbourhoods, and that cuckolding males are often cuckolded themselves. Derived from ecological mechanisms, these new perspectives point towards the evolution of sociality in birds, with relevance also for mammals and primates including humans.

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Section: Discussionsupporting

confidence: 81%

Extra-Pair Mating and Evolution of Cooperative Neighbourhoods

Eliassen

Jørgensen

2014

PLoS ONE

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“…Genetic benefits might manifest themselves in other than the measured traits and/or become apparent at later life stages only [13,16]. In particular, sons sired by an extra-pair mate might inherit the ability to gain extra-pair copulations themselves, thereby increasing their lifetime reproductive success ( [59], but see [60]). Increasing the investment in such highly valuable offspring will pay for mothers, and will amplify differences between EPO and WPO [51,61].…”

Section: Discussionmentioning

confidence: 99%

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

et al. 2011

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Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch ( Taeniopygia guttata ), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype–phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.

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“…We genotyped adult birds and nestlings at eight microsatellite loci (Gerlach et al, 2012a), and determined paternity using the program CERVUS 3.0 (Kalinowski et al, 2007). We determined the sex of each nestling by amplifying the CHD gene on the W and Z chromosomes; males and females are homogametic and heterogametic, respectively (Griffiths et al, 1998).…”

Section: Paternity and Sex Analysismentioning

confidence: 99%

Social Environment Has a Primary Influence on the Microbial and Odor Profiles of a Chemically Signaling Songbird

et al. 2016

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Chemical signaling is an underappreciated means of communication among birds, as may be the potential contributions of symbiotic microbes to animal chemical communication in general. The dark-eyed junco (Junco hyemalis) produces and detects volatile compounds that may be important in reproductive behavior. These compounds are found in preen oil secreted by the uropygial gland, and this gland supports diverse bacterial communities including genera known to produce some of these volatile compounds. We investigated the relative contributions of shared environments and genetic relatedness in shaping juncos' symbiotic bacterial communities, and investigated whether these bacterial communities underlie juncos' chemical signaling behavior. We sampled parents and nestlings at 9 junco nests during one breeding season at Mountain Lake Biological Station in Virginia, USA. From each individual, we collected swabs of the uropygial gland and the cloaca, preen oil, and a small blood sample for paternity testing. We characterized junco bacterial communities through 16S rRNA gene surveys and preen oil volatile compounds via gas chromatography-mass spectrometry. Nest membership and age class had the strongest influence on the structure of bacterial and volatile profiles. We compared father-offspring similarity based on paternity, and nestling similarity in nests containing full siblings and half siblings, and found that relatedness did not noticeably affect bacterial or volatile profiles. While we cannot rule out an influence of genetic relatedness on these profiles, it is clear that shared environments are more influential in shaping bacterial and volatile profiles among juncos. We did not find significant covariation between individual bacterial and volatile profiles. Possible explanations for this result include: (1) bacteria do not underlie volatile production; (2) ample redundancy in volatile production among bacterial types obscures covariation; or (3) the relationship is confounded by the fact that, unlike glands exclusively dedicated to chemical communication, uropygial glands have multiple functions, and symbiotic Whittaker et al.Junco Microbial and Odor Profiles bacteria are hypothesized to contribute to each of these. Therefore, different bacteria may contribute to different phenotypes of the avian holobiont. Future work will include cultivation, metabolomic, genomic, and behavioral assay approaches to tease these scenarios apart.

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Promiscuous mating produces offspring with higher lifetime fitness

Cited by 46 publications

References 52 publications

Extra-Pair Mating and Evolution of Cooperative Neighbourhoods

Extra-Pair Mating and Evolution of Cooperative Neighbourhoods

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Social Environment Has a Primary Influence on the Microbial and Odor Profiles of a Chemically Signaling Songbird

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