Repeated convergent evolution of parthenogenesis in Acariformes (Acari)

Abstract

The existence of old species-rich parthenogenetic taxa is a conundrum in evolutionary biology. Such taxa point to ancient parthenogenetic radiations resulting in morphologically distinct species. Ancient parthenogenetic taxa have been proposed to exist in bdelloid rotifers, darwinulid ostracods, and in several taxa of acariform mites (Acariformes, Acari), especially in oribatid mites (Oribatida, Acari). Here, we investigate the diversification of Acariformes and their ancestral mode of reproduction using 18S rRNA. Because parthenogenetic taxa tend to be more frequent in phylogenetically old taxa of Acariformes, we sequenced a wide range of members of this taxon, including early-derivative taxa of Prostigmata, Astigmata, Endeostigmata, and Oribatida. Ancestral character state reconstruction indicated that (a) Acariformes as well as Oribatida evolved from a sexual ancestor, (b) the primary mode of reproduction during evolution of Acariformes was sexual; however, species-rich parthenogenetic taxa radiated independently at least four times (in Brachychthonioidea (Oribatida), Enarthronota (Oribatida), and twice in Nothrina (Oribatida), (c) parthenogenesis additionally evolved frequently in species-poor taxa, for example, Tectocepheus, Oppiella, Rostrozetes, Limnozetes, and Atropacarus, and (d) sexual reproduction likely re-evolved at least three times from species-rich parthenogenetic clusters, in Crotonia (Nothrina), in Mesoplophora/Apoplophora (Mesoplophoridae, Enarthronota), and in Sphaerochthonius/Prototritia (Protoplophoridae, Enarthronota). We discuss possible reasons that favored the frequent diversification of parthenogenetic taxa including the continuous long-term availability of dead organic matter resources as well as generalist feeding of species as indicated by natural variations in stable isotope ratios.