Holocene climate change promoted allopatric divergence and disjunct geographic distribution in a bee orchid species

Aim: Species with disjunct geographic distributions provide natural opportunities to investigate incipient or recent allopatric divergence. The combination of both genetic and ecological data may be fruitful to decipher the causes of such pattern: i) actual vicariance, ii) successful colonization from one source range to a new range (dispersal, biological introduction) or iii) parallel convergent evolution. Location: Southern France and Northern Spain. Taxon: The bee orchid Ophrys aveyronensis (and its two recognized subspecies O. a. subsp. aveyronensis and O. a. subsp. vitorica) displays a disjunct geographic distribution with two subranges separated by 600 km on both sides of the Pyrenees Mountains. Methods: Through a combination of population genomics and Ecological Niche Modelling (ENM), we investigated the causes of this intriguing biogeographic pattern. Results: The population genomic data demonstrate that all the studied populations exhibit similar patterns of genetic diversity and dramatic decrease in effective size compared to the ancestral population. Significant genetic differentiation and reciprocal monophyly exist between populations of the two subranges of O. aveyronensis, despite a very recent divergence time as young as ca. 1500 generations ago. Moreover, (paleo-)ecological Niche Modelling analyses support that the disjunct geographic distribution of the O. aveyronensis is consistent with a range split of a broad ancestral range, contraction and distinct longitudinal and latitudinal shifts in response to climate warming during the Holocene. Main Conclusion: The congruence of the results obtained from both population genomics and ENM approaches documents how very recent continental allopatric divergence initiated speciation in this system. Ophrys aveyronensis provides a promising opportunity to study the onset of reproductive isolation and parallel evolution following an initial stage of geographic separation in a group with high diversification rate.