Contrasting Patterns of Genetic Differentiation among Blackcaps (Sylvia atricapilla) with Divergent Migratory Orientations in Europe

Mihaela Ilieva,Elisabeth Imhof,Gregor Rolshausen,Wolfgang Fiedler,H. Martin Schaefer,David Serrano,Tomasz Wesołowski,Nikita Chernetsov,Gernot Segelbacher,Keith A. Hobson,Arild Johnsen,Raeann Mettler,Swen C. Renner

doi:10.1371/journal.pone.0081365

Abstract

Migratory divides are thought to facilitate behavioral, ecological, and genetic divergence among populations with different migratory routes. However, it is currently contentious how much genetic divergence is needed to maintain distinct migratory behavior across migratory divides. Here we investigate patterns of neutral genetic differentiation among Blackcap (Sylvia atricapilla) populations with different migratory strategies across Europe. We compare the level of genetic divergence of populations migrating to southwestern (SW) or southeastern (SE) wintering areas with birds wintering in the British Isles following a recently established northwesterly (NW) migration route. The migratory divide between SW and SE wintering areas can be interpreted as a result of a re-colonization process after the last glaciation. Thus we predicted greater levels of genetic differentiation among the SW/SE populations. However, a lack of genetic differentiation was found between SW and SE populations, suggesting that interbreeding likely occurs among Blackcaps with different migratory orientations across a large area; therefore the SW/SE migratory divide can be seen as diffuse, broad band and is, at best, a weak isolating barrier. Conversely, weak, albeit significant genetic differentiation was evident between NW and SW migrants breeding sympatrically in southern Germany, suggesting a stronger isolating mechanism may be acting in this population. Populations located within/near the SW/SE contact zone were the least genetically divergent from NW migrants, confirming NW migrants likely originated from within the contact zone. Significant isolation-by-distance was found among eastern Blackcap populations (i.e. SE migrants), but not among western populations (i.e. NW and SW migrants), revealing different patterns of genetic divergence among Blackcap populations in Europe. We discuss possible explanations for the genetic structure of European Blackcaps and how gene flow influences the persistence of divergent migratory behaviors.

Highlights

Patterns of geographic isolation during the Pleistocene in temperate areas have allowed behavioral, ecological, and genetic divergence among geographically isolated populations in a range of taxa [1,2]
While geographic barriers are instrumental in the formation of initial reproductive isolation, further isolating barriers are needed for continued genetic divergence in the face of gene flow, for example in the case of secondary contact between previously isolated populations at contact zones [6]
By simultaneously characterizing levels of neutral genetic differentiation across the SW/SE migratory divide as well as the NW/SW polymorphism, we investigated two competing hypotheses: 1) if the migratory divide represents an adequate isolating barrier, genetic divergence between SW and SE migrants should be detectable and, given the long history of this divide, would be larger than that found at the novel NW/SW migratory polymorphism; 2) if the migratory divide is an incomplete barrier to gene flow, levels of genetic divergence should be lower across the SW/SE migratory divide compared to the novel NW/SW migratory polymorphism experiencing rapid, adaptive divergence in sympatry [17,18,20]

Summary

Introduction

Patterns of geographic isolation during the Pleistocene in temperate areas have allowed behavioral, ecological, and genetic divergence among geographically isolated populations in a range of taxa [1,2]. While geographic barriers are instrumental in the formation of initial reproductive isolation, further isolating barriers are needed for continued genetic divergence in the face of gene flow, for example in the case of secondary contact between previously isolated populations at contact zones [6]. Migratory divides represent the locations at which populations maintain divergent migratory routes, often originating during periods of allopatry, but can evolve into hybrid zones as a result of secondary contact and interbreeding between populations [7]. If isolating barriers are sufficiently strong to maintain some degree of reproductive isolation between divergent populations, the level of genetic divergence among populations with distinct migratory routes may be high [8]. While migratory behavior does not appear to be a strong isolation barrier, it is among the best examples of a mechanism promoting adaptive microevolution [15,16]. Assortative mating based upon allochronic spring arrival to the breeding grounds can facilitate adaptive microevolution in passerines and promote genetic divergence within sympatric breeding populations [17,18,19,20]

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Conclusion