Parthenogenesis and Sexuality in Oribatid Mites : phylogeny, mitochondrial genome structure and resource dependence

The present thesis investigates molecular and ecological effects of different reproductive modes on oribatid mites as model organisms (Acari, Oribatida). The investigation of the evolution and maintenance of sex vs. parthenogenesis is one of the most exciting fields in evolutionary biology. It is still puzzling why sexual reproduction dominates in the animal kingdom beside its high costs: females need to invest time and resources in searching mating partners and copulation, they dilute their genomes and halve the amount of reproductive progeny by producing males (cost of meiosis + cost of males = twofold costs of sex). Although these costs seem overwhelming, only 1% of all Metazoa reproduce by parthenogenesis. Three so-called “ancient asexual scandals”, namely bdelloid rotifers, darwinulid ostracods and several lineages of oribatid mites, challenge theories on the maintenance of sex as they persist over evolutionary timescales. Oribatid mites are ideal model organisms to investigate molecular and ecological consequences of sex and parthenogenesis. Among the roughly 10,000 mainly soil-dwelling oribatid mite species about 9% are parthenogenetic, a percentage which is unusually high; further, up to 80% of oribatid mite individuals in forest soil reproduce by parthenogenesis. Sexual and parthenogenetic oribatid mites coexist in the same habitat allowing to investigate the role of ecological factors, e.g., the availability of resources. The first study of this thesis aimed at clarifying the relationship of Astigmata and Oribatida which is controversially discussed. We tested the hypothesis that Astigmata evolved from within Desmonomata which renders Oribatida paraphyletic by sequencing two genes (18S, ef1α) for a representative sample of oribatid and astigmatid mite species. Phylogenetic analyses using three different analytical approaches did not support the hypothesis on the origin of Astigmata within Oribatida. Astigmata always clustered outside Oribatida with or close to Endeostigmata, usually in a sister-group relationship. The second study of this thesis investigated phylogenetic positions of sexually vs. parthenogenetically reproducing Desmonomata. Three genes (ef1α, hsp82 and 18S) were sequenced and phylogenetic analyses were performed on a concatenated dataset. Character history and ancestral state evolution analyses revealed that Crotoniidae re-evolved sexuality from the parthenogenetic cluster of Camisiidae. This reversal in reproductive mode is unique in the animal kingdom and violates Dollo’s law that complex ancestral states can never be reacquired. In the third and fourth study of this thesis the complete mitochondrial genomes of the sexual species Steganacarus magnus and the parthenogenetic species Platynothrus peltifer were sequenced. The genome of S. magnus lacks 16 tRNAs and the gene order differs from the hypothetical ancestral chelicerate arrangement as conserved in Limulus polyphemus. The structure of tRNAs differs remarkably from the typical cloverleaf structure which also was the case in P. peltifer. The mitochondrial gene arrangement of P. peltifer differs from the hypothetical ground plan and to the arrangement in S. magnus mainly in the positions of nad1 and nad2. In contrast to our hypothesis, no gene duplication of cox1 was found but single nucleotide polymorphisms causes a low level of intraindividual heteroplasmy that cannot explain the high intraspecific diversity found in other studies. The fifth study of this thesis investigated the re-colonization of soil and litter by sexual and parthenogenetic oribatid mites and their response to resource depletion in laboratory microcosms over ten months. In agreement with our expectations, parthenogenetic taxa suffered more from resource shortage than sexual species. However, the results suggest that the recovery from disturbances and the recolonization of soil and litter is more influenced by body size and generation time than by reproductive mode. In general, egg numbers were higher in sexual than in parthenogenetic species. The results further suggest that parthenogenetic taxa adjusted the investment in reproduction by reducing egg production with declining availability of resources. The sixth experiment of this thesis explored effects of increased availability of high quality resources on the abundance of sexual and parthenogenetic oribatid mite species at different temperatures (10, 15 and 20°C). In contrast to our expectations, species abundances declined in each of the treatments at each temperature and sexuals and parthenogens were equally affected. The results indicate that oribatid mites in the field feed on other resources than easily available carbon, potentially mycorrhizal fungi. Overall, the results of the present thesis expand and strengthen the use of oribatid mites as model organisms in evolutionary biology. The reversal of the reproductive mode in Crotoniidae is unique for “ancient asexuals” and allows the investigation of genetical consequences of sex and parthenogenesis. The presence of spanandric males in parthenogenetic taxa allows investigating factors responsible for the persistence of genes involved in meiosis, sperm production and sex determination. Further topics for future studies comprise the investigation of population structures using microsatellites as neutral markers, the existence transposable elements, and the role of resource quality and quantity for the high frequency of parthenogenesis in soil microarthopods