Dataset Information

Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks.

ABSTRACT: It is well established that differences in migratory behavior between populations of songbirds have a genetic basis but the actual genes underlying these traits remains largely unknown. In an attempt to identify such candidate genes we de novo assembled the genome of the willow warbler Phylloscopus trochilus, and used whole-genome resequencing and a SNP array to associate genomic variation with migratory phenotypes across two migratory divides around the Baltic Sea that separate SW migrating P. t. trochilus wintering in western Africa and SSE migrating P. t. acredula wintering in eastern and southern Africa. We found that the genomes of the two migratory phenotypes lack clear differences except for three highly differentiated regions located on chromosomes 1, 3, and 5 (containing 146, 135, and 53 genes, respectively). Within each migratory phenotype we found virtually no differences in allele frequencies for thousands of SNPs, even when comparing geographically distant populations breeding in Scandinavia and Far East Russia (>6000 km). In each of the three differentiated regions, multidimensional scaling-based clustering of SNP genotypes from more than 1100 individuals demonstrates the presence of distinct haplotype clusters that are associated with each migratory phenotype. In turn, this suggests that recombination is absent or rare between haplotypes, which could be explained by inversion polymorphisms. Whereas SNP alleles on chromosome 3 correlate with breeding altitude and latitude, the allele distribution within the regions on chromosomes 1 and 5 perfectly matches the geographical distribution of the migratory phenotypes. The most differentiated 10 kb windows and missense mutations within these differentiated regions are associated with genes involved in fatty acid synthesis, possibly representing physiological adaptations to the different migratory strategies. The ?200 genes in these regions, of which several lack described function, will direct future experimental and comparative studies in the search for genes that underlie important migratory traits.

SUBMITTER: Lundberg M

PROVIDER: S-EPMC6121796 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks.

Lundberg Max M Liedvogel Miriam M Larson Keith K Sigeman Hanna H Grahn Mats M Wright Anthony A Åkesson Susanne S Bensch Staffan S

Evolution letters 20170616 3

It is well established that differences in migratory behavior between populations of songbirds have a genetic basis but the actual genes underlying these traits remains largely unknown. In an attempt to identify such candidate genes we <i>de novo</i> assembled the genome of the willow warbler <i>Phylloscopus trochilus</i>, and used whole-genome resequencing and a SNP array to associate genomic variation with migratory phenotypes across two migratory divides around the Baltic Sea that separate SW ...[more]

PMID: 30283646

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Project description:INTRODUCTION:In contact zones, genetic mixing of two taxa can be restricted by prezygotic (e.g. assortative mating) or postzygotic (lower fitness of hybrid offspring) barriers, or a combination of the two. A hybrid zone between two willow warbler subspecies (Phylloscopus trochilus trochilus, P. t. acredula) with distinctive migratory strategies occurs in central Sweden. These subspecies exhibit differences in migratory direction and distance, resulting in geographically distinct wintering areas in Africa. The subspecies may have diverged from a common refuge after the last ice age, and neutral genetic markers are homogeneous across their range. By contrast, several phenotypic traits and genetic markers of two chromosomal regions previously identified show steep clines across the divide. The evolutionary forces that maintain this migratory divide remain unknown. Here we use plumage colour, morphology, genetic markers and feather stable nitrogen-isotopes (? (15)N) to assess if assortative mating between migratory phenotypes could be acting as a possible mechanism for keeping the two forms genetically separate and maintaining the migratory divide. We colour-ringed a willow warbler breeding population in the central part of the hybrid zone and observed the breeding population to assess phenotypic and genotypic traits of social pairs. RESULTS:Our data suggest that wintering area and genetic ancestry had an effect on male arrival time to the breeding grounds which could contribute to assortment. However, evidence for assortative mating could not be detected based on a comparison of plumage colour, morphology and ? (15)N between social mates. CONCLUSION:This finding was strengthened by analyses of subspecies-specific genetic markers, which allowed us to identify the presence of a large proportion of potential hybrids and backcrosses at the study site. Our results supported the hypothesis that pre-mating isolation in willow warblers is weak, resulting in extensive hybridisation across the migratory divide.

Project description:Hydrogen isotope analysis of feather keratin (?2HF) has become an essential tool for tracking movements between breeding and wintering populations of migratory birds. In particular, ?2HF has been used to create ?2HF isoscapes that can be used to assign the geographic origins of molt. The majority of past studies have sampled a portion of a single feather as an isotopic proxy for the entire plumage although surprisingly little is known about variation of stable isotopes within and between feather tracts of individuals in local populations. Here we examine ?2HF variation in 24 pterylographic variables (9 primaries, 6 secondaries, 6 rectrices, and 3 patches of ventral contour feathers) in individual specimens of black-throated blue warbler (Setophaga caerulescens) breeding in the Big Santeetlah Creek watershed (5350 ha), southern Appalachian Mountains. By restricting our study to territorial ASY males (after second year) inhabiting a small watershed, we could focus on ?2HF variation generated during the complete prebasic annual molt in a circumscribed population while factoring out age and sexual differences in foraging behavior, isotopic incorporation, and post-breeding dispersal. Summed within-individual variation (?2HF) across 24 pterylographic variables ranged from 12 to 60‰ (= 21.8 ± 9.4‰), with 81% of the individuals exhibiting variation ? 16‰ (reproducibility of analyses was ? 4 ‰). Adjacent feathers in feather tracts tend to have more similar ?2HF values than feathers grown weeks apart, consistent with the stepwise replacement of flight feathers. The pooled population sample exhibited significant ?2HF variation in primaries (-78 to -21‰), secondaries (-80 to -17‰), rectrices (-78 to -23‰), and ventral contour feathers (-92 to -32‰). Strong year effects in ?2HF variation were observed in each of the 24 pterylographic variables. Altitudinal effects were observed only in ventral contour feathers. The current findings demonstrate that within-individual variation (?2HF) may be much greater than previously thought in migratory species that molt on or near breeding territories. Our study also highlights the need for greater pterylographic precision in research design of isotope-based studies of avian movement. Within-individual and within-population ?2HF variation should be incorporated in geographic assignment models. In a broader context, the staggered Staffelmauser pattern of molt in wood warblers provides an exceptional view of the seasonal variation of hydrogen isotopes circulating in blood plasma during the six-week period of annual molt.

Dataset Information

Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks.

Publications

Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks.

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