Many islands are biodiversity hotspots that host numerous endemic species. Unfortunately, insular faunas suffer from high rates of extinction and endangerment, and numerous conservation plans have been developed for their protection. These conservation plans are often assessed on the basis of occurrence and proportion of endemic taxa. However, delimitations of species and subspecies are still confusing and controversial. From a practical point of view, these disagreements make it difficult for government agencies and non‐governmental organizations to initiate conservation measures. The present study develops a pragmatic integrative taxonomic approach on the basis of molecular and eco‐chemical criteria. This method is applied to the insular bumblebee fauna of Corsica. For each taxon, the differentiation of Corsican taxa from the nearest related allopatric parents is characterized using genetic markers and the chemical composition of cephalic labial gland secretions. Phylogenetic analyses, Bayesian implementation of the general mixed Yule‐coalescent approach, and comparative chemical studies show that two Corsican taxa can be considered as endemic species while five others can be considered as subspecies. Regardless of the taxonomic assessment the method facilitates diagnosis of evolutionarily significant units and rank taxa according to their distinctiveness. International Union for Conservation of Nature red lists are reconsidered according to the new taxonomic hypothesis for Corsican bumblebees. Modifications in species assessments are proposed. The present approach provides useful data sets for policy‐makers and conservation organizations.

BackgroundThe Pleistocene climatic oscillations are considered as a major driving force of intraspecific divergence and speciation. During Ice Ages, populations isolated in allopatric glacial refugia can experience differentiation in reproductive traits through divergence in selection regimes. This phenomenon may lead to reproductive isolation and dramatically accentuates the consequences of the climatic oscillations on species. Alternatively, when reproductive isolation is incomplete and populations are expanding again, further mating between the formerly isolated populations can result in the formation of a hybrid zone, genetic introgression or reinforcement speciation through reproductive trait displacements. Therefore changes in reproductive traits driven by population movements during climatic oscillations can act as an important force in promoting pre-zygotic isolation. Notwithstanding, divergence of reproductive traits has not been approached in the context of climatic oscillations. Here we investigate the impact of population movements driven by climatic oscillations on a reproductive trait of a bumblebee species (Bombus lapidarius). We characterise the pattern of variation and differentiation across the species distribution (i) with five genes (nuclear and mitochondrial), and (ii) in the chemical composition of male marking secretions (MMS), a key trait for mate attraction in bumblebees.ResultsOur results provide evidence that populations have experienced a genetic allopatric differentiation, in at least three main refugia (the Balkans, Centre-Eastern Europe, and Southern Italy) during Quaternary glaciations. The comparative chemical analyses show that populations from the Southern Italian refugium have experienced MMS differentiation and an incipient speciation process from another refugium. The meeting of Southern Italian populations with other populations as a result of range expansion at a secondary contact zone seems to have led to a reinforcement process on local MMS patterns.ConclusionsThis study suggests that population movement during Quaternary climatic oscillations can lead to divergence in reproductive traits by allopatric differentiation during Ice Ages and by reinforcement during post-glacial recolonization.

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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.