Radiation in sexual and parthenogenetic oribatid mites (Oribatida, Acari) as indicated by genetic divergence of closely related species

The D3 domain and its flanking regions of 28S rRNA of four pairs of closely related sexual species (Eupelops hirtus and E. torulosus; Oribatella calcarata and O. quadricornuta; Chamobates voigtsi and Ch. borealis; Liacarus coracinus and L. subterraneus) and four pairs of closely related parthenogenetic species (Nanhermannia nana and Na. coronata; Nothrus silvestris and No. palustris; Tectocepheus sarekensis and T. minor; Camisia spinifer and Ca. segnis) of oribatid mites were sequenced to investigate (1) if the D3 region can be used as a species marker and (2) if there is genetic variation among closely related species pairs and if its magnitude is related to reproductive mode. Furthermore, we investigated the world-wide genetic variation of the D3 region from the oribatid mite species Platynothrus peltifer. There was no intraspecific genetic variation in the D3 region in any of the species studied; it was even identical in two closely related parthenogenetic species (Na. nana and Na. coronata) and two closely related sexual species (E. hirtus and E. torulosus). The genetic differences of the other species pairs indicated that both parthenogenetic and sexual lineages have various ages. On average, however, the differences between the closely related parthenogenetic species were larger than those between closely related sexual species, indicating that parthenogenetic lineages exist historically and may radiate slower than sexual species. The findings of this study support the hypothesis that some of the parthenogenetic oribatid mite taxa (Tectocepheus, Nothrus) are ‘ancient asexuals’. The absence of intraspecific or intra-individual variation in the D3 region of parthenogenetic species is consistent with the presence of concerted evolution in the 28S rRNA gene. From this we infer the existence of a meiotic process, which is consistent with the automixy known from several other parthenogenetic oribatid species. This revised version was published online in July 2006 with corrections to the Cover Date.     

Multiple convergent evolution of arboreal life in oribatid mites indicates the primacy of ecology

Frequent convergent evolution in phylogenetically unrelated taxa points to the importance of ecological factors during evolution, whereas convergent evolution in closely related taxa indicates the importance of favourable pre-existing characters (pre-adaptations). We investigated the transitions to arboreal life in oribatid mites (Oribatida, Acari), a group of mostly soil-living arthropods. We evaluated which general force—ecological factors, historical constraints or chance—was dominant in the evolution of arboreal life in oribatid mites. A phylogenetic study of 51 oribatid mite species and four outgroup taxa, using the ribosomal 18S rDNA region, indicates that arboreal life evolved at least 15 times independently. Arboreal oribatid mite species are not randomly distributed in the phylogenetic tree, but are concentrated among strongly sclerotized, sexual and evolutionary younger taxa. They convergently evolved a capitate sensillus, an anemoreceptor that either precludes overstimulation in the exposed bark habitat or functions as a gravity receptor. Sexual reproduction and strong sclerotization were important pre-adaptations for colonizing the bark of trees that facilitated the exploitation of living resources (e.g. lichens) and served as predator defence, respectively. Overall, our results indicate that ecological factors are most important for the observed pattern of convergent evolution of arboreal life in oribatid mites, supporting an adaptationist view of evolution.     

Convergent evolution of defense mechanisms in oribatid mites (Acari, Oribatida) shows no "ghosts of predation past"

Oribatid mites are diverse and abundant terrestrial soil arthropods that are involved in decomposition of organic matter and nutrient cycling. As indicated by fossils starting from the Devonian, they evolved varied mechanisms and structures for defense from predators. We investigated four of these defensive structures (ptychoid body, hologastry, mineralization and opisthonotal glands) and used ancestral character state reconstruction to determine whether they evolved convergently and how many times this may have happened. Phylogenetic trees based on 18S rDNA were constructed for 42 oribatid mite species and two outgroup taxa using likelihood and Bayesian algorithms. The results suggest that at least three of the four defensive structures evolved convergently several times; for opisthonotal glands convergent evolution remains equivocal. This high level of convergence indicates that predation has been an important factor throughout the evolution of oribatid mites, contributing to morphological diversity and potentially also to species richness, as there are indications that some taxa radiated after the evolution of defense structures. Despite the ancientness of oribatid mites, defense structures seems to have been rarely lost, suggesting that they still are functional and necessary to reduce predation, rather than being 'ghosts of predation past'.     

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.     

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

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.     

Convergent evolution of sexual shape dimorphism in Diptera

Several patterns of sexual shape dimorphism, such as male body elongation, eye stalks, or extensions of the exoskeleton, have evolved repeatedly in the true flies (Diptera). Although these dimorphisms may have evolved in response to sexual selection on male body shape, conserved genetic factors may have contributed to this convergent evolution, resulting in stronger phenotypic convergence than might be expected from functional requirements alone. I compared phenotypic variation in body shape in two distantly related species exhibiting sexually dimorphic body elongation: Prochyliza xanthostoma (Piophilidae) and Telostylinus angusticollis (Neriidae). Although sexual selection appears to act differently on male body shape in these species, they exhibited strikingly similar patterns of sexual dimorphism. Likewise, patterns of within-sex shape variation were similar in the two species, particularly in males: relative elongation of the male head capsule, antenna, and legs was associated with reduced head capsule width and wing length, but was nearly independent of variation in thorax length. However, the two species presented contrasting patterns of static allometry: male sexual traits exhibited elevated allometric slopes in T. angusticollis, but not in P. xanthostoma. These results suggest that a shared pattern of covariation among traits may have channeled the evolution of sexually dimorphic body elongation in these species. Nonetheless, static allometries may have been shaped by species-specific selection pressures or genetic architectures.     

The association of oribatid mites with lichens

Oribatei (Acari, Cryptostigmata) are found in a variety of terrestrial habitats, and many are associated with lichens; the relationship ranges from casual to highly dependent. Eighty-three species associated with lichens have been surveyed, and a tentative classification, based on their ecological requirements, is presented: Group A consists of species restricted to lichens as a biotope, though occasionally occurring as accidentals in other habitats; Group B consists of species which while preferring lichens as a habitat and feeding source are also adapted to existence on other plants (though in some cases their immatures may be lichen-restricted); Group C consists of species which, though frequently found on lichens, are equally common in other biotopes, particularly mosses, and must be regarded as much more generalized in their feeding habits. Certain aspects of oribatid-lichen specificity are discussed. The importance of oribatid-lichen associations from the point of view of soil fertility and energetics is emphasized.     

Dispersal patterns of oribatid mites across habitats and seasons

Oribatid mites are tiny arthropods that are common in all soils of the world; however, they also occur in microhabitats above the soil such as lichens, mosses, on the bark of trees and in suspended soils. For understanding oribatid mite community structure, it is important to know whether they are dispersal limited. The aim of this study was to investigate the importance of oribatid mite dispersal using Malaise traps to exclude sole passive wind-dispersal. Oribatid mite communities were collected over a 3-year period from five habitat types (coniferous forests, deciduous forests, mixed forests, meadows, bog/heathlands sites) and three seasons (spring, summer, autumn) in Sweden. Mites entered traps either by walking or by phoresy, i.e., by being attached to flying insects. We hypothesized (1) that oribatid mite communities in the traps differ between habitats, indicating habitat-limited dispersal, and (2) that oribatid mite communities differ among seasons suggesting that dispersal varies due to changing environmental conditions such as moisture or resource availability. The majority of the collected species were not typically soil-living species but rather from habitats such as trees, lichens and mosses (e.g., Carabodes labyrinthicus, Cymbaeremaeus cymba, Diapterobates humeralis and Phauloppia lucorum) indicating that walking into the traps or entering them via phoresy are of greater importance for aboveground than for soil-living species. Overall, oribatid mite communities collected in the traps likely originated from the surrounding local habitat suggesting that long distance dispersal of oribatid mites is scarce. Significant differences among seasons indicate higher dispersal during warm and dry periods of the year. Notably, 16 species of oribatid mites collected in our study were sampled for the first time in Sweden. This study also demonstrates that Malaise traps are a meaningful tool to investigate spatial and temporal patterns of oribatid mite communities.

     

Comparative water relations of sub-Antarctic and continental Antarctic oribatid mites

 Water availability, in addition to cold, is important in limiting biotic distribution in the Antarctic regions. In general, inland continental Antarctic habitats are dry, relative to maritime and sub-Antarctic habitats. This investigation compares the water relations of an endemic continental Antarctic oribatid mite, Maudheimia petronia Wallwork, and two sub-Antarctic oribatid mites, Halozetes fulvus Engelbrecht and Podacarus auberti Grandjean. M. petronia showed enhanced survival of dehydrating conditions, which may be attributable to both its greater resistance to and tolerance of water loss. The estimated lethal exposure times (LT₅₀) for M. petronia, P. auberti and H. fulvus held at 15°C and 0–5% RH were 250, 135 and 51 h, respectively. M. petronia lost water significantly more slowly than the sub-Antarctic mites (P<0.05), which did not differ in their rates of water loss (P>0.05). The mean losses of initial body water content after 45 h were 18.9, 27.3 and 29.3% for M. petronia, P. auberti and H. fulvus, respectively, and lethal water losses causing 50% of the sample to die were 65, 52, and 28%, respectively. These data suggest physiological adaptation by M. petronia for existence in periodically dry “chalikosystem” habitats at Antarctic nunataks. Comparisons of tolerance of submersion in freshwater showed P. auberti to be superior to M. petronia; the LT₅₀ values for submersion were >146 h and 32 h, respectively. Tolerance of submersion by P. auberti may be important for its existence in wet sub-Antarctic habitats. Conversely, the poor tolerance shown by M. petronia suggests that this mite has not been associated with moist environments. Received: 13 April 1995/Accepted: 4 August 1995     

An efficient and non-destructive DNA extraction method for oribatid mites

Molecular methods play an important role in systematic acarology and DNA extraction is the first step in this ground. Nowadays, the varieties of methods are being used for extraction of DNA, but most of them destroy the important external characters that are essential for morphological identification. In order to overcome the problem of associating molecular and morphological information, we have developed a simple, efficient and non-destructive DNA extraction method for oribatid mites. The non-destructive method was tested on three different species [Oppia nitens C.L. Koch, 1836 (Oppiidae), Acrotritia ardua C.L. Koch, 1841 (Euphthiracaridae), and Amerus polonicus Kulczynski, 1902 (Ameridae)] and exoskeleton of specimens were preserved in Hoyer’s medium on glass microscopic slides for further identification via morphological studies. This method is more time consuming than commercial kits, but is easier and cheaper, meanwhile, allows systematic analysis with linking the morphological and genetic traits from a single mite. The most important advantage of TNES method is that after using this non-destructive method, specimens preserve all of their morphological features.     

Temperature effects on locomotor activity rates of sub-Antarctic oribatid mites

The influence of temperature on locomotor activity was determined for the sub-Antarctic mites, Halozetes fulvus Engelbrecht and Podacarus auberti Grandjean. In both species walking was severely impaired at below-freezing temperatures. Above zero, locomotor activity rates increased with a rise in temperature over a wide temperature range (for example, this was 2–30°C for H. fulvus), and they showed a biologically normal level of sensitivity to change in temperature. All the calculated Q₁₀ values for mean rates over 5° intervals varied between 1.3 and 2.9. The present data are compared with some rate functions of maritime and continental Antarctic micro-arthropods, and they confirm the relative enhancement of the physiological rate by a continental Antarctic mite. One explanation for the less temperature-sensitive rates in H. fulvus and P. auberti may be that they have relatively more time available for normal biological activity.     

Overwintering ecology of alpine Collembola and oribatid mites from the Austrian Alps

Abstract. 1. Collembola and oribatid mites from windswept mountain ridges at about 2700 m a.s.l. in the Austrian Alps were all killed by freezing, and depend on supercooling to survive low winter temperatures. The Collembola Tetracanthella afurcata Handschin, Xenylla acauda Gisin and Isotoma spp. collected in January had average supercooling points between -25 and -29°C, and the oribatid mites Fuscozetes fuscipes (Koch) and Lepidozetes singularis Berlese of about -28 and -31°C respectively. The ability to supercool was not increased during storage at -5°C, and was generally lower in species collected in March.
2. The oribatid mites Fuscozetes intermedius Caroli and Maffia, F. fuscipes, Damaeus diversipilis (Willmann) and L.singularis contained from 9 to 16 μg glycerol per mg fresh weight after storage at -5°C, while no glycerol could be detected in the Collembola Isotoma spp., T.afurcata and Onychiurus vontoernei Gisin.
3. Activity below 0°C was observed in T.afurcata and O.vontoernei , which had chill-coma temperatures of -7.7 and -4.9°C respectively.
4. Some specimens of F.intermedius survived more than 90 days of anoxia at 0°C, T.afurcata up to 60 days and O.vontoernei up to 24 days.
5. The overwintering biology of Collembola and oribatid mites from the Austrian Alps appears similar to that of Norwegian species, except that those from Austria have slightly lower supercooling points and higher contents of glycerol.     

Hooker Lecture 1974: Convergent evolution in aquatic fungi: the tetraradiate spore

Fungi are mostly terrestrial. Less than 2% of the species are aquatic. These include primitive species with zoospores (Chytridiomycetes and Oomycetes) and re-migrant types mostly in Ascomycetes and Fungi Imperfecti (including Hyphomycetes) with a very few in Basidio-mycetes. Aquatic Hyphomycetes are abundant on decaying leaves (especially of broad-leaved trees) in well-aerated streams and rivers. Their conidia are hyaline and mostly of unusual form. In many the conidium is tetraradiate consisting of four long arms diverging from a common point. In the different genera the tetraradiate conidium develops in very different ways. In some it is a phialoconidium; in others a thalloconidium. In some attachment to the conidiophore is by the tip of one of the four arms; in others near their point of divergence. In some all arms develop simultaneously; in others in succession. The wide range of developmental geometry suggests convergent evolution. The tetraradiate aquatic spore also occurs in Basidiomycetes. The only two higher Basidiomycetes (both marine) with submerged sporophores have tetraradiate basidiospores. The world-wide distribution of aquatic Hyphomycetes is discussed. Their general ecology is also considered. Concentrations of 1000 to 10,000 conidia per litre may be reached in small rivers in autumn. Attention is paid to the possible biological value of the tetraradiate aquatic spore. The evidence suggests that this is connected with the problem of initial anchorage in the turbulent conditions of a stream.     

Nested patterns of community assembly in the colonisation of artificial canopy habitats by oribatid mites

An observed species–area relationship (SAR) in assemblages of oribatid mites inhabiting natural canopy habitats (suspended soils) led to an experimental investigation of how patch size, height in canopy and moisture influence the species richness, abundance and community composition of arboreal oribatid mites. Colonisation by oribatid mites on 90 artificial canopy habitats (ACHs) of three sizes placed at each of three heights on the trunks of ten western redcedar trees was recorded over a 1‐year period. Fifty‐nine oribatid mite species colonised the ACHs, and richness increased with the moisture content and size of the habitat patch. Oribatid mite species richness and abundance, and ACH moisture content decreased with increasing ACH height in the canopy. Patterns in the species richness and community composition of ACHs were non‐random and demonstrated a significant nested pattern. Correlations of patch size, canopy height and moisture content with community nestedness suggest that species‐specific environmental tolerances combined with the differential dispersal abilities of species contributed to the non‐random patterns of composition in these habitats. In line with the prediction that niche‐selection filters out species from the regional pool that cannot tolerate environmental harshness, moisture‐stressed ACHs in the high canopy had lower community variability than ACHs in the lower canopy. Colonising source pools to ACHs were almost exclusively naturally‐occurring canopy sources, but low levels of colonisation from the forest floor were apparent at low heights within the ACH system. We conclude that stochastic dispersal dynamics within the canopy are crucial to understanding oribatid mite community structure in suspended soils, but that the relative importance of stochastic dispersal assembly may be dependent on a strong deterministic element to the environmental tolerances of individual species which drives non‐random patterns of community assembly.     

Positive correlation of trophic level and proportion of sexual taxa of oribatid mites (Acari: Oribatida) in alpine soil systems

We investigated community structure, trophic ecology (using stable isotope ratios; ¹⁵N/¹⁴N, ¹³C/¹²C) and reproductive mode of oribatid mites (Acari, Oribatida) along an altitudinal gradient (2,050–2,900 m) in the Central Alps (Obergurgl, Austria). We hypothesized that (1) the community structure changes with altitude, (2) oribatid mites span over four trophic levels, (3) the proportion of sexual taxa increases with altitude, and (4) the proportion of sexual taxa increases with trophic level, i.e. is positively correlated with the δ¹⁵N signatures. Oribatid mite community structure changed with altitude indicating that oribatid mites occupy different niches at different altitudes. Oribatid mites spanned over 12 δ¹⁵N units, i.e. about four trophic levels, which is similar to lowland forest ecosystems. The proportion of sexually reproducing taxa increased from 2,050 to 2,900 m suggesting that limited resource availability at high altitudes favors sexual reproduction. Sexual taxa more frequently occurred higher in the food web indicating that the reproductive mode is related to nutrition of oribatid mites. Generally, oribatid mite community structure changed from being decomposer dominated at lower altitude to being dominated by fungal and lichen feeders, and predators at higher altitude. This supports the view that resources from dead organic material become less available with increasing altitude forcing species to feed on living resources such as fungi, lichens and nematodes. Our findings support the hypothesis that limited resource accessibility (at high altitudes) favors sexually reproducing species whereas ample resource supply (at lower altitudes) favors parthenogenetic species.