Narrow hybrid zones in spite of very low population differentiation in neutral markers in an island bird species complex.

Patterns of phenotypic and genic frequencies across hybrid zones provide insight into the origin and evolution of reproductive isolation. The Reunion grey white-eye, Zosterops borbonicus, exhibits parapatrically distributed plumage colour forms across the lowlands of the small volcanic island of Reunion (Mascarene archipelago). These forms meet and hybridize in regions that are natural barriers to dispersal (rivers, lava fields). Here, we investigated the relationship among patterns of differentiation at neutral genetic (microsatellite) markers, phenotypic traits (morphology and plumage colour) and niche characteristics across three independent hybrid zones. Patterns of phenotypic divergence revealed that these hybrid zones are among the narrowest ever documented in birds. However, the levels of phenotypic divergence stand in stark contrast to the lack of clear population neutral genetic structure between forms. The position of the hybrid zones coincides with different natural physical barriers, yet is not associated with steep changes in vegetation and related climatic variables, and major habitat transitions are shifted from these locations by at least 18 km. This suggests that the hybrid zones are stabilized over natural dispersal barriers, independently of environmental boundaries, and are not associated with niche divergence. A striking feature of these hybrid zones is the very low levels of genetic differentiation in neutral markers between forms, suggesting that phenotypic divergence has a narrow genetic basis and may reflect recent divergence at a few linked genes under strong selection, with a possible role for assortative mating in keeping these forms apart.

Conserved G-matrices of morphological and life-history traits among continental and island blue tit populations.

The genetic variance-covariance matrix (G-matrix) summarizes the genetic architecture of multiple traits. It has a central role in the understanding of phenotypic divergence and the quantification of the evolutionary potential of populations. Laboratory experiments have shown that G-matrices can vary rapidly under divergent selective pressures. However, because of the demanding nature of G-matrix estimation and comparison in wild populations, the extent of its spatial variability remains largely unknown. In this study, we investigate spatial variation in G-matrices for morphological and life-history traits using long-term data sets from one continental and three island populations of blue tit (Cyanistes caeruleus) that have experienced contrasting population history and selective environment. We found no evidence for differences in G-matrices among populations. Interestingly, the phenotypic variance-covariance matrices (P) were divergent across populations, suggesting that using P as a substitute for G may be inadequate. These analyses also provide the first evidence in wild populations for additive genetic variation in the incubation period (that is, the period between last egg laid and hatching) in all four populations. Altogether, our results suggest that G-matrices may be stable across populations inhabiting contrasted environments, therefore challenging the results of previous simulation studies and laboratory experiments.

The role of selection and historical factors in driving population differentiation along an elevational gradient in an island bird.

Adaptation to local environmental conditions and the range dynamics of populations can influence evolutionary divergence along environmental gradients. Thus, it is important to investigate patterns of both phenotypic and genetic variations among populations to reveal the respective roles of these two types of factors in driving population differentiation. Here, we test for evidence of phenotypic and genetic structure across populations of a passerine bird (Zosterops borbonicus) distributed along a steep elevational gradient on the island of Réunion. Using 11 microsatellite loci screened in 401 individuals from 18 localities distributed along the gradient, we found that genetic differentiation occurred at two spatial levels: (i) between two main population groups corresponding to highland and lowland areas, respectively, and (ii) within each of these two groups. In contrast, several morphological traits varied gradually along the gradient. Comparison of neutral genetic differentiation (FST ) and phenotypic differentiation (PST ) showed that PST largely exceeds FST at several morphological traits, which is consistent with a role for local adaptation in driving morphological divergence along the gradient. Overall, our results revealed an area of secondary contact midway up the gradient between two major, cryptic, population groups likely diverged in allopatry. Remarkably, local adaptation has shaped phenotypic differentiation irrespective of population history, resulting in different patterns of variation along the elevational gradient. Our findings underscore the importance of understanding both historical and selective factors when trying to explain variation along environmental gradients.

Extremely reduced dispersal and gene flow in an island bird.

The Réunion grey white-eye, Zosterops borbonicus, a passerine bird endemic to Réunion Island in the Mascarene archipelago, represents an extreme case of microgeographical plumage colour variation in birds, with four distinct colour forms occupying different parts of this small island (2512 km(2)). To understand whether such population differentiation may reflect low levels of dispersal and gene flow at a very small spatial scale, we examined population structure and gene flow by analysing variation at 11 microsatellite loci among four geographically close localities (<26 km apart) sampled within the distribution range of one of the colour forms, the brown-headed brown form. Our results revealed levels of genetic differentiation that are exceptionally high for birds at such a small spatial scale. This strong population structure appears to reflect low levels of historical and contemporary gene flow among populations, unless very close geographically (<10 km). Thus, we suggest that the Réunion grey white-eye shows an extremely reduced propensity to disperse, which is likely to be related to behavioural processes.

Heritability estimates from genomewide relatedness matrices in wild populations: Application to a passerine, using a small sample size.

Genomic developments have empowered the investigation of heritability in wild populations directly from genomewide relatedness matrices (GRM). Such GRM-based approaches can in particular be used to improve or substitute approaches based on social pedigree (PED-social). However, measuring heritability from GRM in the wild has not been widely applied yet, especially using small samples and in nonmodel species. Here, we estimated heritability for four quantitative traits (tarsus length, wing length, bill length and body mass), using PED-social, a pedigree corrected by genetic data (PED-corrected) and a GRM from a small sample (n = 494) of blue tits from natural populations in Corsica genotyped at nearly 50,000 filtered SNPs derived from RAD-seq. We also measured genetic correlations among traits, and we performed chromosome partitioning. Heritability estimates were slightly higher when using GRM compared to PED-social, and PED-corrected yielded intermediate values, suggesting a minor underestimation of heritability in PED-social due to incorrect pedigree links, including extra-pair paternity, and to lower information content than the GRM. Genetic correlations among traits were similar between PED-social and GRM but credible intervals were very large in both cases, suggesting a lack of power for this small data set. Although a positive linear relationship was found between the number of genes per chromosome and the chromosome heritability for tarsus length, chromosome partitioning similarly showed a lack of power for the three other traits. We discuss the usefulness and limitations of the quantitative genetic inferences based on genomic data in small samples from wild populations.