Holocene Climate Change Promoted Allopatric Divergence and Disjunct Geographic Distribution in a Bee Orchid Species

ABSTRACT 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 patterns: (i) actual vicariance, (ii) successful colonisation from one source 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 recognised 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 mountain range. Methods As allopatric divergence is often complex to document in the wild, we used a combination of population genomics and ecological niche modelling (ENM) to investigate 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 with 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‐ENM analyses support that the disjunct geographic distribution of 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. O. 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.