Autumn migration direction of juvenile willow warblers (Phylloscopus t. trochilus and P. t. acredula) and their hybrids assessed by qPCR SNP genotyping

Tianhao Zhao,Susanne Åkesson,Kristaps Sokolovskis,Keith Larson,Max Lundberg,Staffan Bensch,Mihaela Ilieva,Júlio M Neto

doi:10.1186/s40462-020-00209-7

Abstract

BackgroundsGeographic regions, where two closely related taxa with different migration routes come into contact, are known as migratory divides. Hybrids originating from migratory divides are hypothesized to migrate intermediately relative to the parental populations. Few studies have tested this hypothesis in wild birds, and only in hybrids that have completed the migration back to the breeding grounds. Here, we make use of the well-established migration routes of willow warblers (Phylloscopus trochilus), for which the subspecies trochilus and acredula have migration-associated genetic markers on chromosomes 1 and 5. The genetic approach enabled us to analyze the geographic distribution of juveniles during their first autumn migration, predicting that hybrids should be more frequent in the central flyway over Italy than along the typical SW routes of trochilus and SE routes of acredula.MethodsBlood and feather samples were collected from wintering birds in Africa (n = 69), and from juveniles during autumn migration in Portugal (n = 33), Italy (n = 38) and Bulgaria (n = 32). Genotyping was carried out by qPCR SNP assays, on one SNP each on chromosome 1 (SNP 65) and chromosome 5 (SNP 285). Both these SNPs have alternative alleles that are highly fixed (> 97%) in each of the subspecies.ResultsThe observed combined genotypes of the two SNPs were associated with the known migration routes and wintering distributions of trochilus and acredula, respectively. We found hybrids (HH) among the juveniles in Italy (5/38) and in Portugal (2/33). The proportion of hybrids in Italy was significantly higher than expected from a background rate of hybrid genotypes (1.5%) in allopatric populations of the subspecies.ConclusionsOur genetic approach to assign individuals to subspecies and hybrids allowed us to investigate migration direction in juvenile birds on their first migration, which should better reflect the innate migratory direction than studies restricted to successful migrants. The excess of hybrids in Italy, suggests that they employ an intermediate route relative to the parental populations. Our qPCR SNP genotyping method is efficient for processing large sample sizes, and will therefore be useful in migration research of species with known population genetic structure.

Highlights

Migratory divides, defined as geographic regions where the ranges of two closely related taxa that differ in migration routes come into contact and interbreed, are described from several avian species in Europe [1], Asia [2] and North America [3]
The observed combined genotypes of the two SNPs were associated with the known migration routes and wintering distributions of trochilus and acredula, respectively
Studies based on stable isotope analyses and tracks from geolocators have the inherited constraint that the wintering areas and migration routes can only be obtained from successfully migrating individuals, i.e. those that managed to return from the winter quarters to the breeding sites

Summary

Introduction

Migratory divides, defined as geographic regions where the ranges of two closely related taxa that differ in migration routes come into contact and interbreed, are described from several avian species in Europe [1], Asia [2] and North America [3]. It has been proposed that migratory divides are maintained by selection against hybrids [1, 3,4,5] This idea is based on the hypothesis that hybrids migrate along an intermediate direction relative to their parents, and that such routes confer lower survival, requiring hybrids to cross major geographical barriers, e.g. oceans (Mediterranean Sea [6]), deserts (Sahara [7]) or mountain ranges (Qinghai-Tibetan Plateau [2]). The first attempts to investigate the migration routes of hybrids in the wild made use of stable isotope analyses of feathers moulted at the wintering grounds [5, 9, 10] These studies suggested that hybrids between two species of flycatchers and between Acrocephalus warblers occupied wintering areas, and presumably used migration routes, that were similar to one of the parental species rather than migrating intermediately. Other approaches are needed to obtain unbiased estimates of migration routes taken by first-time juvenile migratory birds, e.g. genetic tools [16, 17]

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Conclusion