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.
Museum specimens are of particular importance for investigating systematics and the biogeography as well as other aspects of the evolution of biodiversity. They are also a depository of specimens accumulated over recent historical times and often the only way to study recently extinct or rare species. Unfortunately, most museum specimens yield low-quality DNA limiting their generalized use in phylogenetic and population genetic studies. Advances in sequencing technologies now offer opportunities to analyse such material even from very small tissue. Here, we applied the Illumina technology (HiSeq) on three specimens of crowned pigeon (Goura spp.) collected in New Guinea between 1879 and 1934. A shotgun strategy allowed us to quickly and reliably assemble complete mitochondrial genomes and fragments of three single-copy gene phylogenetic markers even with low double-stranded DNA quantity (9 to 69 ng). Phylogenetic assignments of these new sequences confirmed them as Goura sequences. Therefore, our study confirms the power of using next-generation sequencing methods to investigate the evolutionary history of species for which access to fresh samples is limited but museum collections are available. These approaches are considerably increasing the value of many natural history collections for genetic investigations, particularly from biodiversity hotspots that are presently difficult to prospect.
The Ré union 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 (o26 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 (o10 km). Thus, we suggest that the Ré union grey white-eye shows an extremely reduced propensity to disperse, which is likely to be related to behavioural processes.
Understanding the mechanisms responsible for phenotypic diversification within and among species ultimately rests with linking naturally occurring mutations to functionally and ecologically significant traits. Colour polymorphisms are of great interest in this context because discrete colour patterns within a population are often controlled by just a few genes in a common environment. We investigated how and why phenotypic diversity arose and persists in the Zosterops borbonicus white-eye of Reunion (Mascarene archipelago), a colour polymorphic songbird in which all highland populations contain individuals belonging to either a brown or a grey plumage morph. Using extensive phenotypic and genomic data, we demonstrate that this melanin-based colour polymorphism is controlled by a single locus on chromosome 1 with two large-effect alleles, which was not previously described as affecting hair or feather colour. Differences between colour morphs appear to rely upon complex cis-regulatory variation that either prevents the synthesis of pheomelanin in grey feathers, or increases its production in brown ones. We used coalescent analyses to show that, from a ‘brown’ ancestral population, the dominant ‘grey’ allele spread quickly once it arose from a new mutation. Since colour morphs are always found in mixture, this implies that the selected allele does not go to fixation, but instead reaches an intermediate frequency, as would be expected under balancing selection.
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, due to 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 Gmatrices for morphological and life-history traits using long-term data sets from one continental and three island populations of Blue tit (Cyanistes caeruleus), which 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 (i.e. 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.
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.
Recently diverged taxa showing marked phenotypic and ecological diversity provide optimal systems to understand the genetic processes underlying speciation. We used genome‐wide markers to investigate the diversification of the Reunion grey white‐eye (Zosterops borbonicus) on the small volcanic island of Reunion (Mascarene archipelago), where this species complex exhibits four geographical forms that are parapatrically distributed across the island and differ strikingly in plumage colour. One form restricted to the highlands is separated by a steep ecological gradient from three distinct lowland forms which meet at narrow hybrid zones that are not associated with environmental variables. Analyses of genomic variation based on single nucleotide polymorphism data from genotyping‐by‐sequencing and pooled RAD‐seq approaches show that signatures of selection associated with elevation can be found at multiple regions across the genome, whereas most loci associated with the lowland forms are located on the Z sex chromosome. We identified TYRP1, a Z‐linked colour gene, as a likely candidate locus underlying colour variation among lowland forms. Tests of demographic models revealed that highland and lowland forms diverged in the presence of gene flow, and divergence has progressed as gene flow was restricted by selection at loci across the genome. This system holds promise for investigating how adaptation and reproductive isolation shape the genomic landscape of divergence at multiple stages of the speciation process.
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