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Genetic variation in nuclear and mitochondrial markers supports a large sex difference in lifetime reproductive skew in a lekking species.

ABSTRACT: Sex differences in skews of vertebrate lifetime reproductive success are difficult to measure directly. Evolutionary histories of differential skew should be detectable in the genome. For example, male-biased skew should reduce variation in the biparentally inherited genome relative to the maternally inherited genome. We tested this approach in lek-breeding ruff (Class Aves, Philomachus pugnax) by comparing genetic variation of nuclear microsatellites (? n ; biparental) versus mitochondrial D-loop sequences (? m ; maternal), and conversion to comparable nuclear (N e ) and female (N ef ) effective population size using published ranges of mutation rates for each marker (?). We provide a Bayesian method to calculate N e (? n = 4N e ? n ) and N ef (? m = 2N ef ? m ) using 95% credible intervals (CI) of ? n and ? m as informative priors, and accounting for uncertainty in ?. In 96 male ruffs from one population, N e was 97% (79-100%) lower than expected under random mating in an ideal population, where N e :N ef = 2. This substantially lower autosomal variation represents the first genomic support of strong male reproductive skew in a lekking species.

SUBMITTER: Verkuil YI

PROVIDER: S-EPMC4224536 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Genetic variation in nuclear and mitochondrial markers supports a large sex difference in lifetime reproductive skew in a lekking species.

Verkuil Yvonne I YI Juillet Cedric C Lank David B DB Widemo Fredrik F Piersma Theunis T

Ecology and evolution 20140903 18

Sex differences in skews of vertebrate lifetime reproductive success are difficult to measure directly. Evolutionary histories of differential skew should be detectable in the genome. For example, male-biased skew should reduce variation in the biparentally inherited genome relative to the maternally inherited genome. We tested this approach in lek-breeding ruff (Class Aves, Philomachus pugnax) by comparing genetic variation of nuclear microsatellites (θ n ; biparental) versus mitochondrial D-lo ...[more]

PMID: 25478153

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Project description:Genetic analyses based on noninvasively collected samples have become an important tool for evolutionary biology and conservation. Crested macaques (Macaca nigra), endemic to Sulawesi, Indonesia, are important for our understanding of primate evolution as Sulawesi macaques represent an exceptional example of primate adaptive radiation. Crested macaques are also Critically Endangered. However, to date we know very little about their genetics. The aim of our study was to find and validate microsatellite markers useful for evolutionary, conservation, and other genetic studies on wild crested macaques. Using fecal samples of 176 wild macaques living in the Tangkoko Reserve, Sulawesi, we identified 12 polymorphic microsatellite loci through cross-species polymerase chain reaction amplification with later modification of some of these primers. We tested their suitability by investigating and exploring patterns of paternity, observed heterozygosity, and evidence for inbreeding. We assigned paternity to 63 of 65 infants with high confidence. Among cases with solved paternity, we found no evidence of extragroup paternity and natal breeding. We found a relatively steep male reproductive skew B index of 0.330 ± 0.267; mean ± SD) and mean alpha paternity of 65% per year with large variation across groups and years (29-100%). Finally, we detected an excess in observed heterozygosity and no evidence of inbreeding across our three study groups, with an observed heterozygosity of 0.766 ± 0.059 and expected heterozygosity of 0.708 ± 0.059, and an inbreeding coefficient of -0.082 ± 0.035. Our results indicate that the selected markers are useful for genetic studies on wild crested macaques, and possibly also on other Sulawesi and closely related macaques. They further suggest that the Tangkoko population of crested macaques is still genetically variable despite its small size, isolation, and the species' reproductive patterns. This gives us hope that other endangered primate species living in small, isolated populations may also retain a healthy gene pool, at least in the short term.

Project description:BackgroundIn insect societies, intracolonial genetic variation is predicted to affect both colony efficiency and reproductive skew. However, because the effects of genetic variation on these two colony characteristics have been tested independently, it remains unclear whether they are affected by genetic variation independently or in a related manner. Here we test the effect of genetic variation on colony efficiency and reproductive skew in a rhinotermitid termite, Reticulitermes speratus, a species in which female-female pairs can facultatively found colonies. We established colonies using two types of female-female pairs: colonies founded by sisters (i.e., sister-pair colonies) and those founded by females from different colonies (i.e., unrelated-pair colonies). Colony growth and reproductive skew were then compared between the two types of incipient colonies.ResultsAt 15 months after colony foundation, unrelated-pair colonies were larger than sister-pair colonies, although the caste ratio between workers and nymphs, which were alternatively differentiated from young larvae, did not differ significantly. Microsatellite DNA analyses of both founders and their parthenogenetically produced offspring indicated that, in both sister-pair and unrelated-pair colonies, there was no significant skew in the production of eggs, larvae, workers and soldiers. Nymph production, however, was significantly more skewed in the sister-pair colonies than in unrelated-pair colonies. Because nymphs can develop into winged adults (alates) or nymphoid reproductives, they have a higher chance of direct reproduction than workers in this species.ConclusionsOur results support the idea that higher genetic variation among colony members could provide an increase in colony productivity, as shown in hymenopteran social insects. Moreover, this study suggests that low genetic variation (high relatedness) between founding females increases reproductive skew via one female preferentially channeling her relatives along the reproductive track. This study thus demonstrated that, in social insects, intracolonial genetic variation can simultaneously affect both colony efficiency and reproductive skew.

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Genetic variation in nuclear and mitochondrial markers supports a large sex difference in lifetime reproductive skew in a lekking species.

Publications

Genetic variation in nuclear and mitochondrial markers supports a large sex difference in lifetime reproductive skew in a lekking species.

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