Evidence for speciation underground in diving beetles (Dytiscidae) from a subterranean archipelago

Most subterranean animals are assumed to have evolved from surface
ancestors following colonisation of a cave system, however very few
studies have raised the possibility of ‘subterranean speciation’ in
underground habitats (i.e. obligate cave-dwelling organisms (troglobionts)
descended from troglobiotic ancestors). Numerous endemic subterranean
diving beetle species from spatially-discrete calcrete aquifers in Western
Australia (stygobionts) have evolved independently from surface ancestors;
however, several cases of sympatric sister species raises the possibility
of subterranean speciation. We tested this hypothesis using vision
(phototransduction) genes that are evolving under neutral processes in
subterranean species and purifying selection in surface species. Using
sequence data from 32 subterranean and five surface species in the genus
Paroster (Dytiscidae), we identified deleterious mutations in: long
wavelength opsin (lwop), arrestin 1 (arr1), and arrestin 2 (arr2) shared
by a sympatric sister-species triplet, arr1 shared by a sympatric
sister-species pair, and lwop and arr2 shared among closely related
species in adjacent calcrete aquifers. In all cases, a common ancestor
possessed the function-altering mutations, implying they were already
adapted to aphotic environments. Our study represents one of the first
confirmed cases of subterranean speciation in cave insects. The assessment
of genes undergoing pseudogenisation provides a novel way of testing modes
of speciation and the history of diversification in blind cave animals.