Walking alone to the north: The origin and historical expansion of the polyploid parthenogenetic lineage in a weevil

Abstract

Background Polyploid parthenogenetic organisms are distributed nonrandomly with respect to their diploid sexual relatives, and this pattern has been well documented in plants. Comparable cases are rare in animals, and the genomic origins of such lineages have been reconstructed in only a few taxa. Additional animal examples are therefore needed to distinguish general eco-evolutionary processes from taxonomic idiosyncrasies. Results We determined the sex of 2,223 individuals of the flightless weevil Catapionus nebulosus species group from 294 localities across Japan. The sex ratio shifted sharply toward females in northern Japan. Phylogenetic analyses using mitochondrial and genome-wide SNP data assigned all female-only populations to a single lineage, which arose through hybridization between two divergent sexual lineages and then expanded rapidly in both range and population size. Flow cytometry showed that the females were tetraploid or pentaploid, and virgin females reared in isolation produced fertile female offspring. In the sexual populations, larval density and individual heterozygosity both declined toward the northern range margin. These declines began south of the co-occurrence zone with the parthenogenetic lineage. Conclusions The all-female lineage of the Catapionus nebulosus species group is a polyploid parthenogen of single hybrid origin. It expanded toward the northern range margin, where sexual populations were sparse or absent. This pattern is consistent with mate limitation, as described in Baker's law. Polyploidy, hybrid origin, and asexuality coincide with a poleward range in this weevil as they do in many plants. The syndrome is therefore not confined to plants, and this weevil offers a valuable animal system for studying the eco-evolutionary processes that generate such distributions.