Independently Evolving Species in Asexual Bdelloid Rotifers

Abstract

Asexuals are an important test case for theories of why species exist. If asexual clades displayed the same pattern of discrete variation as sexual clades, this would challenge the traditional view that sex is necessary for diversification into species. However, critical evidence has been lacking: all putative examples have involved organisms with recent or ongoing histories of recombination and have relied on visual interpretation of patterns of genetic and phenotypic variation rather than on formal tests of alternative evolutionary scenarios. Here we show that a classic asexual clade, the bdelloid rotifers, has diversified into distinct evolutionary species. Intensive sampling of the genus Rotaria reveals the presence of well-separated genetic clusters indicative of independent evolution. Moreover, combined genetic and morphological analyses reveal divergent selection in feeding morphology, indicative of niche divergence. Some of the morphologically coherent groups experiencing divergent selection contain several genetic clusters, in common with findings of cryptic species in sexual organisms. Our results show that the main causes of speciation in sexual organisms, population isolation and divergent selection, have the same qualitative effects in an asexual clade. The study also demonstrates how combined molecular and morphological analyses can shed new light on the evolutionary nature of species. The evolution of distinct species has often been considered a property solely of sexually reproducing organisms. In fact, however, there is little evidence as to whether asexual groups do or do not diversify into species. We show that a famous group of asexual animals, the bdelloid rotifers, has diversified into distinct species broadly equivalent to those found in sexual groups. We surveyed diversity within a single clade, the genus Rotaria, from a range of habitats worldwide, using DNA sequences and measurements of jaw morphology from scanning electron microscopy. New statistical methods for the combined analysis of morphology and DNA sequence data confirmed two fundamental properties of species, namely, independent evolution and ecological divergence by natural selection. The two properties did not always coincide to define unambiguous species groups, but this finding is common in sexual groups as well. The results show that sex is not a necessary condition for speciation. The methods offer the potential for increasing our understanding of the nature of species boundaries across a wide range of organisms.