Molecular phylogeny of oribatid mites (Oribatida, Acari): evidence for multiple radiations of parthenogenetic lineages

Abstract

Nucleotide sequences of the D3 expansion segment and its flanking regions of the 28S rDNA gene were used to evaluate phylogenetic relationships among representative sexual and asexual oribatid mites (Oribatida, Acariformes). The aim of this study was to investigate the hypothesis that oribatid mites consist of species-rich clusters of asexual species that may have radiated while being parthenogenetic. Furthermore, the systematic position of the astigmate mites (Astigmata, Acariformes) which have been hypothesised to represent a paedomorphic lineage within the oribatid mites, is investigated. This is the first phylogenetic tree for oribatid mites s.l. (incl. Astigmata) based on nucleotide sequences. Intraspecific genetic variation in the D3 region was very low, confirming the hypothesis that this region is a good species marker. Results from neighbour joining (NJ) and maximum parsimony (MP) algorithms indicate that several species-rich parthenogenetic groups like Camisiidae, Nanhermanniidae and Malaconothridae are monophyletic, consistent with the hypothesis that some oribatid mite groups diversified despite being parthenogenetic. The MP and maximum likelihood (ML) method indicated that the D3 region is a good tool for elucidating the relationship of oribatid mite species on a small scale(genera, families) but is not reliable for large-scale taxonomy, because branches from the NJ algorithm collapsed in the MP and ML tree. In all trees calculated by different algorithms the Astigmata clustered within the oribatid mites, as proposed earlier.

Reevolution of sexuality breaks Dollo's law

“…All algorithms gave nearly identical tree topologies, which largely agree with those based on morphological data and earlier molecular studies ( Fig. 1) (9,19,20). Although Desmonomata as a whole were paraphyletic, all internal taxa except Camisiidae were monophyletic.…”

“…Much of what has been written about large parthenogenetic clusters in oribatid mites has focused on Desmonomata (9,10,14), especially Camisiidae, Malaconothridae, and Trhypochthoniidae. Our data support monophyly of species-rich parthenogenetic taxa within Desmonomata and therefore that parthenogenetic lineages of oribatid mites are not evolutionary ''dead-ends''; they have persisted and radiated to form clusters, e.g., the parthenogenetic genus Nothrus with 67 species.…”

“…Members of Enarthronota and Mixonomata were sequenced for use as respective outgroups and were selected on the basis of earlier phylogenetic studies (9,19,20). Parhyposomata and Palaeosomata were not included, because they are small taxa having no apparent bearing on our objectives.…”

“…Why this is not true has been debated for decades, with so many answers having been proposed (3-5) that a second enigma has emerged: How could a few animal lineages have maintained parthenogenetic reproduction over considerable evolutionary time, avoiding extinction long enough to radiate and form monophyletic clades? The most studied examples of such ''ancient asexual scandals'' (1) are darwinulid ostracods (6), bdelloid rotifers (7), and several large clusters within oribatid mites (8)(9)(10)(11).…”

“…An estimated 9% of species are parthenogenetic, which is one to two orders of magnitude higher than in other animal groups (8). Most parthenogenetic oribatid mites are clustered in species-rich clades with no known sexual species, making each such clades an independent ''asexual scandal'' (8,9,11,14).…”