Abstract

BackgroundAcross heterogeneous environments selection and gene flow interact to influence the rate and extent of adaptive trait evolution. This complex relationship is further influenced by the rarely considered role of phenotypic plasticity in the evolution of adaptive population variation. Plasticity can be adaptive if it promotes colonization and survival in novel environments and in doing so may increase the potential for future population differentiation via selection. Gene flow between selectively divergent environments may favour the evolution of phenotypic plasticity or conversely, plasticity itself may promote gene flow, leading to a pattern of trait differentiation in the presence of gene flow. Variation in sensory traits is particularly informative in testing the role of environment in trait and population differentiation. Here we test the hypothesis of ‘adaptive differentiation with minimal gene flow’ in resting echolocation frequencies (RF) of Cape horseshoe bats (Rhinolophus capensis) across a gradient of increasingly cluttered habitats.ResultsOur analysis reveals a geographically structured pattern of increasing RF from open to highly cluttered habitats in R. capensis; however genetic drift appears to be a minor player in the processes influencing this pattern. Although Bayesian analysis of population structure uncovered a number of spatially defined mitochondrial groups and coalescent methods revealed regional-scale gene flow, phylogenetic analysis of mitochondrial sequences did not correlate with RF differentiation. Instead, habitat discontinuities between biomes, and not genetic and geographic distances, best explained echolocation variation in this species. We argue that both selection for increased detection distance in relatively less cluttered habitats and adaptive phenotypic plasticity may have influenced the evolution of matched echolocation frequencies and habitats across different populations.ConclusionsOur study reveals significant sensory trait differentiation in the presence of historical gene flow and suggests roles for both selection and plasticity in the evolution of echolocation variation in R. capensis. These results highlight the importance of population level analyses to i) illuminate the subtle interplay between selection, plasticity and gene flow in the evolution of adaptive traits and ii) demonstrate that evolutionary processes may act simultaneously and that their relative influence may vary across different environments.

Highlights

  • Across heterogeneous environments selection and gene flow interact to influence the rate and extent of adaptive trait evolution

  • We detected no significant interaction between sex and population (GLM, F18, 486 = 1.1, P > 0.05), suggesting that the degree of sexual dimorphism in resting echolocation frequencies (RF) was identical across populations

  • The inclusion of Normalized Difference Vegetation Index (NDVI) in the second stage of the regression model significantly increased the proportion of variance explained in the model (Δ R2 = 0.68, F1, 149 = 528.7.9, P < 0.0001), with NDVI accounting for 80% of the variation in RF (R2 = 0.80, F2, 149 = 310.9, P < 0.0001) after controlling for the effect of body size (Figure 4)

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Summary

Introduction

Across heterogeneous environments selection and gene flow interact to influence the rate and extent of adaptive trait evolution This complex relationship is further influenced by the rarely considered role of phenotypic plasticity in the evolution of adaptive population variation. In populations inhabiting heterogeneous environments adaptive trait divergence in the absence of gene flow is both predicted by theoretical models [1,2,3] and supported by a large number of studies demonstrating a generally negative relationship between levels of population connectivity and the degree of adaptive divergence in the traits under study [4,5,6,7,8] This phenomenon is centred on there are minimal costs to immigration, even nominal gene flow could constrain the evolution of trait variation and lineage divergence [17]. High gene flow between heterogeneous environments may favour the evolution of increased phenotypic plasticity, over adaptive genetic divergence, because it would promote adaptation to new conditions within one or two generations [18,29]. Plasticity would allow a population or individuals to persist long enough in a new environment for selection to bring about the evolution of adaptation to the new environment by acting on the standing genetic variation among individuals [18,23]

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