Genome variation in three Anthophora bee species reflects divergent demographic histories

Population genomics can aid our understanding of the trends and drivers of biodiversity loss but it is still unclear how best to use measures of genome variation to understand population vulnerability in insect species. In particular, it is difficult to disentangle the effects of recent population history and life history on genetic diversity. Here we generate highly contiguous genome assemblies of three species of solitary bee from the genus Anthophora. These species have similar life histories but show contrasting population trends in northern Europe in the last century. Two species, Anthophora plagiata and Anthophora retusa, have experienced declines and recoveries of different magnitudes whereas a third species, Anthophora quadrimaculata, has relative population stability. We use these genome assemblies to study genome variation in 136 samples of these species collected throughout Sweden. In line with previous studies, our phylogenetic analysis indicates that the species diverged ~42 million years ago. We find exceedingly low genetic variation in A. plagiata, a species that has experienced a severe recent bottleneck, but high genetic variation in A. retusa, despite a similar recent population trajectory. Fragmented populations of the threatened species A. plagiata appear isolated from each other, but in A.retusa there is a lack of deep population structure despite the presence of geographically separated subpopulations, reflecting recent connectivity. We infer population size in the distant past using MSMC2 and recent past using GONe. These methods are remarkably concordant, and suggest that there have been ancient fluctuations in population size dating back to the pleistocene with moderate expansions in the past century. These results concord with some other studies of endangered insect species that appear to have experienced population declines that predate the modern era. We also detect long blocks of identity-by-state in A. plagiata, indicative of severe recent inbreeding. We suggest that translocations between isolated populations of this species could have a positive effect on their resilience.