Genetic consequences of social structure in the golden-crowned sifaka

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Abstract
Many species are structured in social groups (SGs) where individuals exhibit complex mating strategies. Yet, most population genetic studies ignore SGs either treating them as small random-mating units or focusing on a higher hierarchical level (the population). Empirical studies acknowledging SGs have found an overall excess of heterozygotes within SGs and usually invoke inbreeding avoidance strategies to explain this finding. However, there is a lack of null models against which ecological theories can be tested and inbreeding avoidance quantified. Here, we investigate inbreeding (deviation from random mating) in an endangered forest-dwelling pair-living lemur species (Propithecus tattersalli). In particular, we measure the inbreeding coefficient (FIS) in empirical data at different scales: SGs, sampling sites and forest patches. We observe high excess of heterozygotes within SGs. The magnitude of this excess is highly dependent on the sampling scheme: while offspring are characterised by a high excess of heterozygotes (FIS < 0), the reproductive pair does not show dramatic departures from Hardy–Weinberg expectations. Moreover, the heterozygosity excess disappears at larger geographic scales (sites and forests). We use a modelling framework that incorporates details of the sifaka mating system but does not include active inbreeding avoidance mechanisms. The simulated data show that, although apparent “random mating” or even inbreeding may occur at the “population” level, outbreeding is maintained within SGs. Altogether our results suggest that social structure leads to high levels of outbreeding without the need for active inbreeding avoidance mechanisms. Thus, demonstrating and measuring the existence of active inbreeding avoidance mechanisms may be more difficult than usually assumed.

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