Abstract
Populations on islands often exhibit lower levels of genetic variation and ecomorphological divergence compared to their mainland relatives. While phenotypic differentiation in characters, such as size or shape among insular organisms, has been well studied, insular differentiation in quantitative reproductive traits involved in chemical communication has received very little attention to date. Here, we investigated the impact of insularity on two syntopic bumblebee species pairs: one including species that are phylogenetically related (Bombus terrestris and B. lucorum), and the other including species that interact ecologically (B. terrestris and its specific nest inquiline B. vestalis). For each bumblebee species, we characterized the patterns of variation and differentiation of insular (Corsican) vs. mainland (European) populations (i) with four genes (nuclear and mitochondrial, 3781 bp) and (ii) in the chemical composition of male marking secretions (MMS), a key trait for mate attraction in bumblebees, by gas chromatography-mass spectrometry (GC-MS). Our results provide evidence for genetic differentiation in Corsican bumblebees and show that, contrary to theoretical expectations, island populations of bumblebees exhibit levels of genetic variation similar to the mainland populations. Likewise, our comparative chemical analyses of MMS indicate that Corsican populations of bumblebees are significantly differentiated from the mainland yet they hold comparative levels of within-population MMS variability compared to the mainland. Therefore, insularity has led Corsican populations to diverge both genetically and chemically from their mainland relatives, presumably through genetic drift, but without a decrease of genetic diversity in island populations. We hypothesize that MMS divergence in Corsican bumblebees was driven by a persistent lack of gene flow with mainland populations and reinforced by the preference of Corsican females for sympatric (Corsican) MMS. The impoverished Corsican bumblebee fauna has not led to relaxation of stabilizing selection on MMS but to consistent differentiation chemical reproductive traits on the island.
Highlights
Islands have always been of particular interest for evolutionary biologists and ecologists alike
All phylogenetic analyses (maximum parsimony (MP), maximum likelihood (ML) and Bayesian methods (MB)) performed on the same dataset led to similar tree topologies and to identical relationships between Corsican and continental taxa
Phylogenetic analyses based on nuclear datasets recovered all deep hierarchical levels relationships among subgenera and between species but EF-1a failed to discriminate between B. lucorum and B. terrestris
Summary
Islands have always been of particular interest for evolutionary biologists and ecologists alike. Theory predicts that reduced immigration rates from mainland, founder events and genetic drift [2,6] generally result in island populations being genetically impoverished compared to their mainland counterparts [7,8,9]. Populations confined to geographically-isolated and contrasting habitats on islands often experience ecomorphological divergence from their mainland relatives. This divergence could result from genetic changes (founder effects or drift) and/or from post-colonization adaptive changes produced by different selection regimes compared to the adjacent mainland habitats [1,2,10,11,12,13,14,15]
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