Parthenogenetic Oribatid Mite Research Articles

"Jack-of-all-trades" is parthenogenetic.

Sex is evolutionarily more costly than parthenogenesis, evolutionary ecologists therefore wonder why sex is much more frequent than parthenogenesis in the majority of animal lineages. Intriguingly, parthenogenetic individuals and species are as common as or even more common than sexuals in some major and putative ancient animal lineages such as oribatid mites and rotifers. Here, we analyzed oribatid mites (Acari: Oribatida) as a model group because these mites are ancient (early Paleozoic), widely distributed around the globe, and include a high number of parthenogenetic species, which often co‐exist with sexual oribatid mite species. There is evidence that the reproductive mode is phylogenetically conserved in oribatid mites, which makes them an ideal model to test hypotheses on the relationship between reproductive mode and species' ecological strategies. We used oribatid mites to test the frozen niche variation hypothesis; we hypothesized that parthenogenetic oribatid mites occupy narrow specialized ecological niches. We used the geographic range of species as a proxy for specialization as specialized species typically do have narrower geographic ranges than generalistic species. After correcting for phylogenetic signal in reproductive mode and demonstrating that geographic range size has no phylogenetic signal, we found that parthenogenetic lineages have a higher probability to have broader geographic ranges than sexual species arguing against the frozen niche variation hypothesis. Rather, the results suggest that parthenogenetic oribatid mite species are more generalistic than sexual species supporting the general‐purpose genotype hypothesis. The reason why parthenogenetic oribatid mite species are generalists with wide geographic range sizes might be that they are of ancient origin reflecting that they adapted to varying environmental conditions during evolutionary history. Overall, our findings indicate that parthenogenetic oribatid mite species possess a widely adapted general‐purpose genotype and therefore might be viewed as “Jack‐of‐all‐trades.”

How land-use intensity affects sexual and parthenogenetic oribatid mites in temperate forests and grasslands in Germany

Intensive land use has been shown to alter the composition and functioning of soil communities. Due to their low dispersal ability, oribatid mites are particularly vulnerable to land-use intensification and species which are not adjusted to management-related disturbances become less abundant. We investigated how different land-use parameters in forests and grasslands affect oribatid mite diversity and abundance, with a focus on: (1) species-level impacts, by classifying species as increasing (‘winners’) or decreasing (‘losers’) in abundance with higher land-use intensity, and (2) reproductive impact, by investigating whether sexual and parthenogenetic species react differently. We collected 32,542 adult oribatid mites in 60 forests and grasslands of known land-use intensity in two regions of Germany. Diversity and total abundance as well as the proportion of sexual species were higher in forests than in grasslands. Diversity declined with higher land-use intensity in forests, but increased with higher mowing and fertilization in grasslands. Depending on land-use parameter and region, abundance either declined or remained unaffected by increasing intensity. Gravidity was higher in sexual than in parthenogenetic species and sexuals had 1.6× more eggs per gravid female. Proportions of sexual species and gravid females decreased with land-use intensity in forests, but increased with mowing in grasslands. At the species level, 75% of sexuals and 87.5% of parthenogens were ‘losers’ of higher percentages of dead wood originating from management-related disturbances. Across land-use parameters and habitats, a similar proportion of sexual and parthenogenetic oribatid mite species were ‘losers’ of high land-use intensity. However, ‘winner’ species were more common among sexuals.

Phylogenetic analysis based on the 16S rDNA, gltA, gatB, and hcpA gene sequences of Wolbachia from the novel host Ceratozetes thienemanni (Acari: Oribatida)

We determined the occurrence of intracellular endosymbionts (Wolbachia, Cardinium, Arsenophonus, Rickettsia, Spiroplasma, Hamiltonella, flavobacteria, and microsporidia) in oribatid mites (Acari: Oribatida) with the use of PCR technique. For the first time we looked for and detected Wolbachia in parthenogenetic oribatid mite Ceratozetes thienemanni Willmann, 1943. The 16S rDNA, gatB, hcpA, and gltA sequences of Wolbachia in C. thienemanni showed the highest similarity (≥ 90%) to the genes of Wolbachia from springtails (Collembola) and oribatid mite Gustavia microcephala. We found the unique sequence 5’-GGGGTAATGGCC-3′ in 16S rDNA of Wolbachia from C. thienemanni and collembolan representing group E. The phylogeny of Wolbachia based on the analysis of single genes as well as concatenated alignments of four bacterial loci showed that the bacteria from C. thienemanni belonged to Wolbachia group E, like the endosymbionts from springtail hosts and G. microcephala. Considering coexisting of representatives of Oribatida and Collembola in the same soil habitat and similar food, it is possible that the source of Wolbachia infection was the same. Residues of dead invertebrates could be in organic matter of their soil food, so the scenario of infection transferred by eating of remains of soil cohabitates is also possible. It could explain the similarity and relationship of the Wolbachia in these two arthropod groups. Oribatid mite C. thienemanni is a parthenogenetic mite which is a unique feature in the genus Ceratozetes. Moreover, this species, within the entire genus Ceratozetes, is characterized by the most northerly distribution. It is difficult to determine either it is parthenogenesis or the presence of endosymbionts that are in some way responsible for this kind of evolutionary success. Maybe we are dealing here with a kind of synergy of both factors?

Temporal fluctuations in oribatid mites indicate that density-independent factors favour parthenogenetic reproduction

We investigated the oribatid mite density, community structure and the percentage of parthenogenetic individuals in four different forest types across three regions in Germany in 2008 and once again in 2011. We compared temporal (inter-annual) fluctuations in population densities between sexually and parthenogenetically reproducing species of oribatid mites. We hypothesized that population densities in parthenogenetic oribatid mite species fluctuate more than in sexual ones. Further, we expected species composition and dominance of parthenogenetic species to differ between forest types and regions. Oribatid mite community structure did not differ between years but varied with forest type and region, indicating low species turnover in time. As hypothesized, temporal fluctuations were more pronounced in parthenogenetic as compared to sexual species. The percentage of parthenogenetic individuals was significantly higher in coniferous than in beech forests and significantly higher in Schorfheide-Chorin than in Hainich-Dün and Schwäbische Alb. The results indicate that parthenogenetic species flourish if populations are controlled by density-independent factors and dominate at sites were resources are plentiful and easily available, such as coniferous forests, and in regions with more acidic soils and thick organic layers, such as Schorfheide-Chorin. However, historical factors also may have contributed to the increased dominance of parthenogenetic species in the Schorfheide-Chorin, as this region was more heavily glaciated and this may have favoured parthenogenetic species. Overall, our study supports the hypothesis that parthenogenetic species benefit from the lack of density-dependent population control whereas the opposite is true for sexual species.

Oribatid mite communities on the bark of dead wood vary with log type, surrounding forest and regional factors

Dead wood is a crucial component of natural and semi-natural forest ecosystems. It is of eminent importance as habitat for a variety of animal species but its importance for microarthropods, a diverse group of small forest animals, has been little studied. We investigated how oribatid mite density, species richness, community structure and the proportion of parthenogenetic individuals on the bark of dead wood are affected by log type (beech, oak) and surrounding forest type (deciduous, coniferous) in three regions in Germany (Schorfheide-Chorin, Hainich-Dün, Schwäbische Alb). Additionally, we analyzed the trophic structure of oribatid mites from the bark of dead wood in one region (Hainich-Dün) using stable isotope ratios (15N/14N, 13C/12C). Oribatid mite richness and community structure were significantly affected by log type, forest type and region. Oribatid mite communities comprised mainly soil and arboreal species but only few dead wood specialists indicating that dead wood in an early stage of decay functions as transitory habitat rather than specific microhabitat. However, some oribatid mites likely are adapted to dead wood as habitat by living phoretically on bark beetles (e.g., Siculobata leontonycha) or endophagous in fungi associated with dead wood (e.g., juvenile Carabodes species). The proportion of parthenogenetic oribatid mite individuals was rather low (∼8%) suggesting that oribatid mites on dead wood predominantly rely on living food resources resembling arboreal communities but not those in soil. Natural variations in stable isotope ratios indicate that oribatid mites on the bark of dead wood span at least three trophic levels including lichen feeders, moss feeders, decomposers and fungal feeders with fungal feeders dominating.

Evidence for frozen-niche variation in a cosmopolitan parthenogenetic soil mite species (Acari, Oribatida).

Parthenogenetic lineages may colonize marginal areas of the range of related sexual species or coexist with sexual species in the same habitat. Frozen-Niche-Variation and General-Purpose-Genotype are two hypotheses suggesting that competition and interclonal selection result in parthenogenetic populations being either genetically diverse or rather homogeneous. The cosmopolitan parthenogenetic oribatid mite Oppiella nova has a broad ecological phenotype and is omnipresent in a variety of habitats. Morphological variation in body size is prominent in this species and suggests adaptation to distinct environmental conditions. We investigated genetic variance and body size of five independent forest - grassland ecotones. Forests and grasslands were inhabited by distinct genetic lineages with transitional habitats being colonized by both genetic lineages from forest and grassland. Notably, individuals of grasslands were significantly larger than individuals in forests. These differences indicate the presence of specialized genetic lineages specifically adapted to either forests or grasslands which coexist in transitional habitats. Molecular clock estimates suggest that forest and grassland lineages separated 16-6 million years ago, indicating long-term persistence of these lineages in their respective habitat. Long-term persistence, and morphological and genetic divergence imply that drift and environmental factors result in the evolution of distinct parthenogenetic lineages resembling evolution in sexual species. This suggests that parthenogenetic reproduction is not an evolutionary dead end.

Resource availability as driving factor of the reproductive mode in soil microarthropods (Acari, Oribatida).

The availability of high quality resources is an important factor driving community structure and reproductive mode of animals. Parthenogenetic reproduction prevails when resources are available in excess, whereas sexuality correlates with resource shortage. We investigated the effect of resource availability on the community structure of oribatid mites in a laboratory experiment. Availability of food resources was increased by addition of glucose to leaf litter and reduced by leaching of nutrients from leaf litter. Experimental systems were incubated at three different temperatures to establish different regimes of resource exploitation. Community structure of oribatids and numbers of eggs per female were measured over a period of ten months. We expected the density of oribatid mites to decline in the reduced litter quality treatment but to increase in the glucose treatment. Both effects were assumed to be more pronounced at higher temperatures. We hypothesized sexual species to be less affected than parthenogenetic species by reduced resource quality due to higher genetic diversity allowing more efficient exploitation of limited resources, but to be outnumbered by parthenogenetic species in case of resource addition due to faster reproduction. In contrast to our hypotheses, both sexual and parthenogenetic oribatid mite species responded similarly with their densities declining uniformly during incubation. The parthenogenetic Brachychthoniidae and Tectocepheus dominated early in the experiment but were replaced later by parthenogenetic Desmonomata and Rhysotritia. In parthenogenetic species the number of eggs per female increased during the experiment while the number of eggs in sexual females remained constant or decreased slightly; in general, egg numbers were higher in sexual than in parthenogenetic species. The results indicate that for sustaining oribatid mite populations other resources than litter and associated saprotrophic microorganisms are needed. They also indicate that there are two groups of parthenogenetically reproducing species: exploiters of easily available resources and consumers of leaf litter associated resources.

Management intensity affects traits of soil microarthropod community in montane spruce forest

This study examined the influence of forest management intensity (3 unmanaged, 3 mild managed, 5 intensively managed stands) on soil microarthropods in montane spruce forest. We particularly focused on Oribatida and Collembola which play important roles in organic matter decomposition and nutrient cycling. Our results showed a significant shift from fungivory and carnivory to detritivory in the Oribatida community accompanying management intensification. Similarly, parthenogenetic oribatid mite species contributed more to the community in intensively managed forests and the presence of Collembola species with developed furca increased with management intensification. Although there was no remarkable influence of management intensity on total densities or diversity indices, important and significant shifts in species composition and functional groups showed that soil functions and processes were affected by forest management. Trait assessment indicates a shift in roles Oribatida play in decomposition; fragmentation and comminuting of undecomposed litter seems to gain importance in the intensively managed forest, whereas fungivorous species affect primary decomposers through feeding on fungi in the unmanaged forest.

The oviduct is a brood chamber for facultative egg retention in the parthenogenetic oribatid mite Archegozetes longisetosus AOKI (Acari, Oribatida)

Archegozetes longisetosus is a parthenogenetic oribatid mite and a chelicerate model organism. We examined the localisation of processes between vitellogenesis and embryogenesis as well as the anatomy and histology of involved structures by means of light- and electron microscopy. The proximal oviduct is differentiated into an oviductal bulb, exhibiting a strong secretory epithelium. Here, solidification of the egg shell instantaneously occurs upon passing of the egg from the perivitelline space into the oviductal lumen. This is interpreted as an internalised oviposition with the generation boundary being effectively located at the ovary–oviduct transition, rendering the oviducts into functional brood chambers. The parity mode combines elements of oviparity and ovolarviparity with facultative egg retention.

Integrative taxonomy: Combining morphological, molecular and chemical data for species delineation in the parthenogenetic Trhypochthonius tectorum complex (Acari, Oribatida, Trhypochthoniidae).

BackgroundThere is a long-standing controversial about how parthenogenetic species can be defined in absence of a generally accepted species concept for this reproductive mode. An integrative approach was suggested, combining molecular and morphological data to identify distinct monophyletic entities. Using this approach, speciation of parthenogenetic lineages was recently demonstrated for groups of bdelloid rotifers and oribatid mites. Trhypochthonius tectorum, an oribatid mite from the entirely parthenogenetic desmonomatan family Trhypochthoniidae, is traditionally treated as a single species in Central Europe. However, two new morphological lineages were recently proposed for some Austrian populations of T. tectorum, and were described as novel subspecies (T. silvestris europaeus) or form (T. japonicus forma occidentalis). We used the morphological and morphometrical data which led to this separation, and added mitochondrial and nuclear DNA sequences and the chemical composition of complex exocrine oil gland secretions to test this taxonomical hypothesis. This is the first attempt to combine these three types of data for integrative taxonomical investigations of oribatid mites.ResultsWe show that the previous European species T. tectorum represents a species complex consisting of three distinct lineages in Austria (T.tectorum, T. silvestris europaeus and T. japonicus forma occidentalis), each clearly separated by morphology, oil gland secretion profiles and mitochondrial cox1 sequences. This diversification happened in the last ten million years. In contrast to these results, no variation among the lineages was found in the nuclear 18S rDNA.ConclusionsOur approach combined morphological, molecular and chemical data to investigate diversity and species delineation in a parthenogenetic oribatid mite species complex. To date, hypotheses of a general oribatid mite phylogeny are manifold, and mostly based on single-method approaches. Probably, the integrative approach proposed here can be used to uncover further hidden biodiversity of glandulate Oribatida and help to build up more stable phylogenetic hypotheses in the future.

Cryptic diversification in ancient asexuals: evidence from the bdelloid rotifer Philodina flaviceps

Bdelloid rotifers, darwinulid ostracods and some oribatid mites have been called 'ancient asexuals' as they speciated and survived over long-term evolutionary timescale without sexual recombination. Data on their genetic diversification are contrasting: within-species diversification is present mostly at a continental scale in a parthenogenetic oribatid mite, whereas almost no genetic diversification at all seems to occur within darwinulid ostracod species. Strangely enough, no clear data for bdelloid rotifers are available so far. In this paper, we analyse partial COI mtDNA sequences to show that a bdelloid rotifer, Philodina flaviceps, so far considered a single traditional morphological species, has actually been able to diversify into at least nine distinct evolutionary entities, with genetic distances between lineages comparable with those between different traditional species within the same genus. We discovered that local coexistence of such different independent lineages is very common: up to four lineages were found in a same stream, and up to three in a single moss sample of 5 cm(2). In contrast to the large-scale geographic pattern that has recently been reported in the oribatid mite, the spatial distribution of the bdelloid lineages provided evidence of micro-phylogeographic patterns. If the mtDNA diversity indicates that the lineages are independent and represent sympatric cryptic species within P. flaviceps, then the actual bdelloid diversity can be expected to be much greater than that recognized today.

Speciation in the parthenogenetic oribatid mite genus Tectocepheus (Acari, Oribatida) as indicated by molecular phylogeny

Summary Despite the lack of universal concepts for species and speciation, both sexual and asexual organisms are expected to diversify into discrete genotypic and morphological clusters. Species-rich clusters of parthenogenetic oribatid mites likely evolved in the absence of sexual reproduction. We used nucleotide sequences of the large and small rDNA genes (18S and 28S) and the coding genes for heat shock protein 82 ( hsp82 ) and elongation factor-1 alpha ( ef-1α ) for phylogenetic analyses of three morphotypes of the parthenogenetic oribatid mite genus Tectocepheus . DNA sequence divergences of the different morphotypes were similar to those of sexual species in other organisms. Maximum likelihood analyses of single genes and combined data sets were largely congruent in reconstructing the phylogeny of the Tectocepheus species. The results suggest that the different morphotypes of Tectocepheus indeed evolved in the absence of sexual reproduction, and that Tectocepheus minor , Tectocepheus velatus and Tectocepheus sarekensis are best considered distinct species. Further, the results suggest that 18S rDNA, hsp82 and ef-1α are powerful markers for resolving phylogenetic relationships of oribatid mites. Saturation plots indicated that the D3-region of 28S is much more saturated than all other examined genes. This indicates that the D3-region is unsuitable for resolving ancient splits in oribatid mites.

High genetic divergences indicate ancient separation of parthenogenetic lineages of the oribatid mite Platynothrus peltifer (Acari, Oribatida)

Theories on the evolution and maintenance of sex are challenged by the existence of ancient parthenogenetic lineages such as bdelloid rotifers and darwinulid ostracods. It has been proposed that several parthenogenetic and speciose taxa of oribatid mites (Acari) also have an ancient origin. We used nucleotide sequences of the mitochondrial gene cytochrome oxidase I to estimate the age of the parthenogenetic oribatid mite species Platynothrus peltifer. Sixty-five specimens from 16 sites in North America, Europe and Asia were analysed. Seven major clades were identified. Within-clade genetic distances were below 2 % similar to the total intraspecific genetic diversity of most organisms. However, distances between clades averaged 56 % with a maximum of 125 %. We conclude that P. peltifer, as it is currently conceived, has existed for perhaps 100 million years, has an extant distribution that results from continental drift rather than dispersal and was subject to several cryptic speciations.

Resources and sex: Soil re-colonization by sexual and parthenogenetic oribatid mites

Factors responsible for the dominance of sexual reproduction in Metazoa are controversial. Generally, the mode of reproduction is correlated with ecological factors: under resource-limited conditions sexual taxa dominate, whereas theoretically parthenogenetic species prevail in stable habitats. To investigate if sexual or parthenogenetic taxa are more affected by environmental conditions, we analyzed (1) the effect of resource depletion on the density of sexual and parthenogenetic oribatid mite taxa and (2) the re-colonization of defaunated soil and litter by sexual and parthenogenetic taxa. In both experiments, the number of eggs in parthenogenetic and sexual species was counted. For the first experiment, laboratory microcosms were established where resources declined with time; for the second experiment, microcosms were defaunated by heat and inoculated with fresh soil and litter material, respectively, as resource for re-colonization by oribatid mites. We hypothesized that parthenogenetic species will suffer more from resource limitation compared to sexual taxa, and that they will colonize habitable space faster due to their faster mode of reproduction. In agreement with our hypothesis, parthenogenetic taxa suffered more from resource limitation than sexual species. In contrast, in the re-colonization experiment the proportion of parthenogenetic taxa remained constant in the treatment re-colonized from soil as well as from litter, indicating that parthenogenetic species are not faster colonizers. In general, egg numbers were higher in sexual species than in parthenogenetic species.

No evidence for the ‘Meselson effect’ in parthenogenetic oribatid mites (Oribatida, Acari)

It has been hypothesized that in ancient apomictic, nonrecombining lineages the two alleles of a single copy gene will become highly divergent as a result of the independent accumulation of mutations (Meselson effect). We used a partial sequence of the elongation factor-1alpha (ef-1alpha) and the heat shock protein 82 (hsp82) genes to test this hypothesis for putative ancient parthenogenetic oribatid mite lineages. In addition, we tested if the hsp82 gene is fully transcribed by sequencing the cDNA and we also tested if there is evidence for recombination and gene conversion in sexual and parthenogenetic oribatid mite species. The average maximum intra-specific divergence in the ef-1alpha was 2.7% in three parthenogenetic species and 8.6% in three sexual species; the average maximum intra-individual genetic divergence was 0.9% in the parthenogenetic and 6.0% in the sexual species. In the hsp82 gene the average maximum intra-individual genetic divergence in the sexual species Steganacarus magnus and in the parthenogenetic species Platynothrus peltifer was 1.1% and 1.2%, respectively. None of the differences were statistically significant. The cDNA data indicated that the hsp82 sequence is transcribed and intron-free. Likelihood permutation tests indicate that ef-1alpha has undergone recombination in all three studied sexual species and gene conversion in two of the sexual species, but neither process has occurred in any of the parthenogenetic species. No evidence for recombination or gene conversion was found for sexual or parthenogenetic oribatid mite species in the hsp 82 gene. There appears to be no Meselson effect in parthenogenetic oribatid mite species. Presumably, their low genetic divergence is due to automixis, other homogenizing mechanisms or strong selection to keep both the ef-1alpha and the hsp82 gene functioning.