Social family structure and biogeography contribute to genomic divergence and cryptic speciation in the only eusocial beetle species,Austroplatypus incompertus(Curculionidae: Platypodinae)

Abstract

Eusociality in insects has arisen multiple times independently in Hymenoptera (bees, wasps, ants), Blattodea (termites) and Coleoptera (beetles). In Hymenoptera and Blattodea, the evolution of eusociality led to massive species proliferation. In the hyperdiverse Coleoptera, eusociality evolved only once, in the ancient Australian ambrosia beetle species Austroplatypus incompertus (Curculionidae: Platypodinae). This species occurs in mesic eucalypt forests of eastern Australia, from Victoria to northern New South Wales. Based on few individuals collected from the southern and northern edges of the species distribution it was initially described as two distinct species; however, the names were later synonymised as no morphological differences were found in analyses of more specimens. Recent mitochondrial haplotype analyses revealed substantial latitudinal divergence across the distribution of A. incompertus. To address this apparent disparity between morphological and molecular data, we sequenced and analysed a SNP panel of over 6,656 biallelic markers from 187 individuals of 11 sites across 1000 km of this species range. Our data indicate that eusocial demographic processes such as low colony establishment success rate, limited dispersal and reliance on few reproductive individuals, together with substantial habitat fragmentation contributed to the population genetic structure of this species. We further identified that the Hunter Valley biogeographic barrier split the species into two distinct clades, with both clades in secondary close contact on the Barrington Tops plateau without any discernible admixture. Our results support the resurrection of a second species of Austroplatypus which has important consequences for the evolution eusociality in Coleoptera and the systematics of Platypodinae.