Genetic and phenotypic divergence in an island bird: isolation by distance, by colonization or by adaptation?

Lewis G Spurgin,Deborah A Dawson,Tove H Jorgensen,David S Richardson,Juan Carlos Illera

doi:10.1111/mec.12672

Abstract

Discerning the relative roles of adaptive and nonadaptive processes in generating differences among populations and species, as well as how these processes interact, is a fundamental aim in biology. Both genetic and phenotypic divergence across populations can be the product of limited dispersal and gradual genetic drift across populations (isolation by distance), of colonization history and founder effects (isolation by colonization) or of adaptation to different environments preventing migration between populations (isolation by adaptation). Here, we attempt to differentiate between these processes using island populations of Berthelot's pipit (Anthus berthelotii), a passerine bird endemic to three Atlantic archipelagos. Using microsatellite markers and approximate Bayesian computation, we reveal that the northward colonization of this species ca. 8500years ago resulted in genetic bottlenecks in the colonized archipelagos. We then show that high levels of genetic structure exist across archipelagos and that these are consistent with a pattern of isolation by colonization, but not with isolation by distance or adaptation. Finally, we show that substantial morphological divergence also exists and that this is strongly concordant with patterns of genetic structure and bottleneck history, but not with environmental differences or geographic distance. Overall, our data suggest that founder effects are responsible for both genetic and phenotypic changes across archipelagos. Our findings provide a rare example of how founder effects can persist over evolutionary timescales and suggest that they may play an important role in the early stages of speciation.

Highlights

Understanding the processes that drive differentiation among populations is a major aim in evolutionary biology
The two tests employed to detect genetic bottlenecks yielded concordant results: there was no evidence for a bottleneck in any of the Canary Island populations, whereas there was a bottleneck signal in the Selvagens, and in all three Madeiran Islands (Table 1)
Pairwise genetic and morphological distance matrices were strongly correlated (R = 0.59, P < 0.001), and again this relationship remained strong and significant when controlling for archipelago effects (R = 0.51, P < 0.001; Figure S3, Supporting information), and for geographic distance (R = 0.58, P < 0.001). We show that these latter two archipelagos were colonized independently from the Canary Islands between 1000 and 26 000 years ago. Both basic population genetic analyses and Bayesian simulations indicate that the patterns of structure observed across the island populations are the result of these dispersal events, with genetic bottlenecks having occurred in the two most recently colonized archipelagos

Summary

Introduction

Understanding the processes that drive differentiation among populations is a major aim in evolutionary biology. Several authors have questioned whether patterns of neutral genetic differentiation can be understood in terms of migration and drift alone and have suggested that selection can play a role In cases where populations exist along environmental gradients, individuals are likely to be adapted to local conditions This local adaptation may act as a barrier to migration, and subsequent drift will result in neutral genetic structure across populations. This phenomenon, known as ‘isolation by adaptation’, has received both theoretical and empirical support, and a recent review suggests that it may be substantially more common than previously realized (Orsini et al 2013b). Because drift is usually considered a null hypothesis, its role in shaping differences among populations and species remains poorly understood (Marie Curie SPECIATION Network 2012)

Methods

Results

Conclusion