Genetic consequences of social structure in the golden-crowned sifaka.

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.

Evidence of genetic monogamy in the lemur Indri (Indri indri).

Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair-living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra-pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair-living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra-pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair-living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair-living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species.