Biogeography and social family structure contribute to cryptic genomic divergence in the only obligate eusocial beetle species, Austroplatypus incompertus (Curculionidae: Platypodinae)

Eusociality in insects has arisen multiple times independently in Hymenoptera (bees, wasps and ants), Blattodea (termites) and Coleoptera (beetles). In Hymenoptera and Blattodea, the evolution of eusociality led to species proliferation. In the hyperdiverse Coleoptera, obligate eusociality evolved only once, in the ancient Australian ambrosia beetle Austroplatypus incompertus (Curculionidae: Platypodinae). This species occurs patchily in mesic eucalypt forests of eastern Australia, from Victoria to northern New South Wales, and has a low dispersal capacity. Based on individuals collected from the southern and northern edges of its distribution, it was initially described as two distinct species. However, the names were later synonymised as no morphological differences were found throughout the species' distribution. Recent mitochondrial analyses revealed substantial latitudinal divergence across populations. To address this disparity between morphological and molecular data, we sequenced and analysed a SNP panel of over 6656 biallelic markers from 187 individuals from 11 sites across 1000 km of this species' range. Our data indicate that eusocial demographic processes such as limited dispersal and reliance on few reproductive individuals, together with habitat fragmentation, contributed to the genetic structuring of this species into northern, central and southern lineages. We further identified low levels of introgression between the highly diverged central and northern lineages at a site close to the Hunter Valley biogeographic barrier, possibly due to secondary contact. Our results highlight the interplay of biogeography and life history on the genomic divergence in this unique ambrosia beetle lineage of important standing in the evolution of eusociality in insects.