Evolutionary history of an island endemic, the Azorean common quail.

Oceanic islands are characterized by conditions that favour diversification into endemic lineages that can be very different from their mainland counterparts. This can be the result of fast phenotypic divergence due to drift or the result of slower adaptation to local conditions. This uniqueness can obscure their evolutionary history. Here we used morphological, stable isotope, genetic and genomic data to characterize common quails (Coturnix coturnix) in the Azores archipelago and assess the divergence from neighbouring common quail populations. Historical documents suggested that these quails could have a recent origin associated with the arrival of humans in the last centuries. Our results show that Azorean quails constitute a well-differentiated lineage with small size and dark throat pigmentation that has lost the migratory ability and that diverged from mainland quail lineages more than 0.8 mya, contrary to the notion of a recent human-mediated arrival. Even though some Azorean quails carry an inversion that affects 115 Mbp of chromosome 1 and that has been associated with the loss of the migratory behaviour in other common quail populations, half of the analysed individuals do not have that inversion and still do not migrate. The long coexistence and evolution in isolation in the Azores of two chromosomal variants (with and without the inversion) is best explained by balancing selection. Thus, a unique and long evolutionary history led to the island endemic that we know today, C. c. conturbans.

Massive genome inversion drives coexistence of divergent morphs in common quails.

The presence of population-specific phenotypes often reflects local adaptation or barriers to gene flow. The co-occurrence of phenotypic polymorphisms that are restricted within the range of a highly mobile species is more difficult to explain. An example of such polymorphisms is in the common quail Coturnix coturnix, a small migratory bird that moves widely during the breeding season in search of new mating opportunities, following ephemeral habitats,1,2 and whose females may lay successive clutches at different locations while migrating.3 In spite of this vagility, previous studies reported a higher frequency of heavier males with darker throat coloration in the southwest of the distribution (I. Jiménez-Blasco et al., 2015, Int. Union Game Biol., conference). We used population genomics and cytogenetics to explore the basis of this polymorphism and discovered a large inversion in the genome of the common quail. This inversion extends 115 Mbp in length and encompasses more than 7,000 genes (about 12% of the genome), producing two very different forms. Birds with the inversion are larger, have darker throat coloration and rounder wings, are inferred to have poorer flight efficiency, and are geographically restricted despite the high mobility of the species. Stable isotope analyses confirmed that birds carrying the inversion have shorter migratory distances or do not migrate. However, we found no evidence of pre- or post-zygotic isolation, indicating the two forms commonly interbreed and that the polymorphism remains locally restricted because of the effect on behavior. This illustrates a genomic mechanism underlying maintenance of geographically structured polymorphisms despite interbreeding with a lineage with high mobility.

Biased assessment of ongoing admixture using STRUCTURE in the absence of reference samples.

Detection of hybridization and introgression is important in ecological research as in conservation and evolutionary biology. STRUCTURE is one of the most popular software to study introgression and allows estimating what proportion of the genome of each individual belongs to each ancestral population, even in cases where no reference sample from the ancestral nonadmixed populations is previously identified. In spite of its frequent use, some studies have indicated that ancestry estimates may not always be reliable. We simulated population data under different conditions with regard to the genetic differentiation between ancestral populations, number of loci considered, number of alleles per marker and hybridization rate, and analysed data with STRUCTURE. When reference samples were not included, the comparison of the known degree of admixture for each simulated individual and the value estimated with STRUCTURE revealed a strong underestimation of the level of introgression, classifying many admixed individuals as nonadmixed. This derives from an inaccurate estimation of the ancestral allele frequencies. When samples from the nonadmixed ancestral population were included as reference in the analyses, the bias in the estimations was reduced. The most accurate estimates were obtained when potentially admixed samples were few in relation to reference samples. Thus, whenever possible, a very large proportion of nonadmixed reference samples should be included in admixture assessments and different approaches should be combined. The misestimate of the amount of introgression can impair our understanding of the evolutionary history of species and misguide conservation efforts.