Genomics Reveal Population Crash and Range Contraction in Elusive Fijian Hylaeus Bees

The conservation of pollinators is of particular interest due to their keystone role in ecosystem function, but is hindered by systematic geographic and methodological biases such that baseline data are not often readily available. Islands are useful as simplified systems to understand evolutionary processes, are known to host higher bee species richness per unit area than mainland regions, and have disproportionate representation of threatened species. We used low-lying and canopy sampling paired with mitochondrial and genomic data to assess a recently discovered clade of canopy-specialist Fijian Hylaeus bees. We found inter-island genetic structure-or incipient speciation-requiring further systematic research. In the most abundant species, H. navai, we used genome-wide SNPs with demographic reconstruction to infer major declines of ~99% (81.6%-99.9% most- to least-conservative, respectively) in effective population size since European colonisation. Over three separate 10-year periods in H. navai's demographic history we inferred population size declines of 61%, 76% and 82%. These declines provide evidence to justify an International Union for Conservation of Nature (IUCN) assessment, with population size declines of this magnitude aligning with criteria for a listing of Critically Endangered. We found evidence of low observed heterozygosity and elevated inbreeding, consistent with a genetic bottleneck. We used species distribution models to show that H. navai has suitable habitat encompassing 1.4%-2.4% of Fiji's land area and is likely now restricted to high elevation forests. By examining historic collections, we raise concerns about contemporary displacement from lowland areas. We suggest that habitat modification (due to increasing human population), the invasive African tulip tree (a potential ecological trap), cyclones, and increased competition from native and introduced pollinators might all interact to drive declines. Our findings are likely not restricted to Fijian bees and provide empirical evidence of declines in hidden canopy pollinators that should be a priority for assessment across the Pacific and the world.