Phylogenomics of Unusual Histone H2A Variants in Bdelloid Rotifers

Rotifers of Class Bdelloidea are remarkable in having evolved for millions of years, apparently without males and meiosis. In addition, they are unusually resistant to desiccation and ionizing radiation and are able to repair hundreds of radiation-induced DNA double-strand breaks per genome with little effect on viability or reproduction. Because specific histone H2A variants are involved in DSB repair and certain meiotic processes in other eukaryotes, we investigated the histone H2A genes and proteins of two bdelloid species. Genomic libraries were built and probed to identify histone H2A genes in Adineta vaga and Philodina roseola, species representing two different bdelloid families. The expressed H2A proteins were visualized on SDS-PAGE gels and identified by tandem mass spectrometry. We find that neither the core histone H2A, present in nearly all other eukaryotes, nor the H2AX variant, a ubiquitous component of the eukaryotic DSB repair machinery, are present in bdelloid rotifers. Instead, they are replaced by unusual histone H2A variants of higher mass. In contrast, a species of rotifer belonging to the facultatively sexual, desiccation- and radiation-intolerant sister class of bdelloid rotifers, the monogononts, contains a canonical core histone H2A and appears to lack the bdelloid H2A variant genes. Applying phylogenetic tools, we demonstrate that the bdelloid-specific H2A variants arose as distinct lineages from canonical H2A separate from those leading to the H2AX and H2AZ variants. The replacement of core H2A and H2AX in bdelloid rotifers by previously uncharacterized H2A variants with extended carboxy-terminal tails is further evidence for evolutionary diversity within this class of histone H2A genes and may represent adaptation to unusual features specific to bdelloid rotifers.     

On the reality and recognisability of asexual organisms: morphological analysis of the masticatory apparatus of bdelloid rotifers

Species concepts and definitions have been a long-standing debate in evolutionary biology since before Darwin, and almost all proposed solutions are based upon grouping and clustering, with species conceived as somehow biological distinct entities, originated and maintained mainly by reproductive isolation. Lacking reproductive exchange, asexual organisms such as bdelloid rotifers, the best-supported clade of so-called 'ancient asexuals', pose an interesting challenge to debates over the reality of species. However, few data are available on bdelloid rotifers. The only evidence has been that bdelloid species have been more consistently recognised than in their sister sexual group, the monogonont rotifers, across successive taxonomic treatments, but this is confounded by the much lesser degree of taxonomic interest in bdelloids. We applied geometric morphometrics analyses on shape and size of hard masticatory pieces, named trophi, of 1420 bdelloids, belonging to 48 populations of eight traditional species, to test the hypothesis of recognisability of bdelloids. Our morphological analysis confirms that traditional bdelloid species are separated distinct entities, possessing trophi morphologies divided by gaps between taxa, similar to patterns of morphological features in sexually reproducing organisms. In common with most microscopic understudied organisms, bdelloid rotifers harbour much previously undescribed diversity: we found significant differences in trophi morphology within traditional species, revealing the existence of cryptic taxa, similar to those also found in facultatively sexual monogonont rotifers. We confirm that recognisability in bdelloids is not qualitatively different from other small understudied animals such as monogononts, and that sexual versus asexual reproduction does not lead to differences in morphological diversity patterns, as previously suggested based on interpretation of taxonomic revisions.     

落叶生境蛭态轮虫物种多样性及四种中国新记录种

为研究落叶生境蛭态轮虫物种多样性,对中国8省28个落叶样品进行了调查,采样范围涵盖中国热带、亚热带及温带地区,海拔高度从3m到1500m不等,共记录蛭态轮虫3科8属29种,其中中国新记录属1属,中国新记录种4种,将中国蛭态轮虫记录由88种增加到92种.研究获取了新记录种跛足突盘轮虫(Bradyscela clauda ...     

Desiccation‐tolerance in bdelloid rotifers facilitates spatiotemporal escape from multiple species of parasitic fungi

Asexuality has major theoretical advantages over sexual reproduction. Nevertheless, obligately asexual metazoan lineages seldom endure over evolutionary time. The Red Queen hypothesis posits that their limited capacity to generate genetic novelty leads to extermination by rapidly evolving parasites and pathogens. At first glance, rotifers of the class Bdelloidea appear to contradict this view: they have reproduced asexually for over 30 Myr without being overwhelmed by parasites. However, there are special ecological conditions under which Red Queen models can accommodate this unusual outcome. If hosts disperse rapidly within a structured metapopulation during a parasite‐free life stage, then in principle they can become spatiotemporally decoupled from coevolving antagonists, and persist without sex. Intriguingly, bdelloid rotifers form dormant propagules when desiccated, which disperse easily by wind. In previous experiments, 7 days of desiccation and wind dispersal removed a fungal parasite from populations of one bdelloid species, allowing them to disperse independently. Here, I extend this finding to two additional bdelloid species and five more fungal parasites, and demonstrate its robustness under various desiccation regimes, and in the presence of multiple parasites. Results support the hypothesis that the unusual physiology of anciently asexual bdelloid rotifers helps them escape fungal parasites in space and time. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 564–574.     

Patterns of diversity in microscopic animals: are they comparable to those in protists or in larger animals?

Aim General patterns of biodiversity, such as latitudinal gradients and species‐area relationships, are found consistently in a wide range of organisms, but recent results for protist diversity suggest that organisms shorter than 2 mm do not display such patterns. We tested this prediction in bdelloid rotifers, pluricellular metazoans smaller than 2 mm, but with size and ecology comparable to protists. Location A single valley in northern Italy was surveyed in detail and compared to all available faunistic data on bdelloids worldwide. Methods We analysed 171 local assemblages of bdelloid rotifers living in 5 systems of dry mosses and submerged mosses in running water and in lakes. We compared patterns of alpha, beta, and gamma diversity, and nestedness of metacommunities, with those known from protists and larger organisms. Results Bdelloid rotifers showed low local species richness (alpha diversity), with strong habitat selection, as observed in larger organisms. The number of species differed among systems, with a higher number of species in dry than in aquatic mosses. There was no hierarchical structure or exclusion of species in the metacommunity pattern within each system. Local diversity for the entire valley was surprisingly high compared with worldwide bdelloid diversity, similar to observed patterns in protists. Main Conclusions Bdelloid rotifers have some of the peculiarities of protist biodiversity, although at slightly different spatial scales, thus confirming the idea of a major change in biodiversity patterns among organisms shorter than 2 mm. However, bdelloids show stronger habitat selection than protists. We suggest two possible explanations for the observed patterns: (1) dispersal is very rare, and not all bdelloid clones are arriving everywhere; and (2) dispersal is effective in displacing propagules, but environmental heterogeneity is very high and prevents many species from colonizing a given patch of moss.     

Pyrophosphate and Ethylenediaminetetraacetate as Relaxants for Lower Invertebrates Prior to Fixation

The method is based on the use of substances that can stop muscular contraction, such as chelants of calcium (EDTA) or known plasticizer of muscle (such as Na₄P₂O₇). Saturated aqueous Na₄P₂O₇ solution and 0.01 M EDTA were used at a room temperature of 22 C. A standard time of 3 hr was required for the substance to have full effect. The method was successfully tested on bdelloid rotifers and subsequently on rotifers other than bdelloid, gastrotrichs, tardigrades, amoebae and vorticellids.     

SEXUAL SPECIES ARE SEPARATED BY LARGER GENETIC GAPS THAN ASEXUAL SPECIES IN ROTIFERS

Why organisms diversify into discrete species instead of showing a continuum of genotypic and phenotypic forms is an important yet rarely studied question in speciation biology. Does species discreteness come from adaptation to fill discrete niches or from interspecific gaps generated by reproductive isolation? We investigate the importance of reproductive isolation by comparing genetic discreteness, in terms of intra‐ and interspecific variation, between facultatively sexual monogonont rotifers and obligately asexual bdelloid rotifers. We calculated the age (phylogenetic distance) and average pairwise genetic distance (raw distance) within and among evolutionarily significant units of diversity in six bdelloid clades and seven monogonont clades sampled for 4211 individuals in total. We find that monogonont species are more discrete than bdelloid species with respect to divergence between species but exhibit similar levels of intraspecific variation (species cohesiveness). This pattern arises because bdelloids have diversified into discrete genetic clusters at a faster net rate than monogononts. Although sampling biases or differences in ecology that are independent of sexuality might also affect these patterns, the results are consistent with the hypothesis that bdelloids diversified at a faster rate into less discrete species because their diversification does not depend on the evolution of reproductive isolation.     

An ecological study of an Antarctic freshwater pool with particular reference to Tardigrada and Rotifera

Deep Lake Tarn is a small pool in the Vestfold Hills, Antarctica, which freezes solid seasonally. When free water is present, rotifers, tardigrades, nematodes, protozoans and bacteria are active and are mainly associated with an algal mat composed of cyanophytes, chlorophytes chrysophytes and a pyrrophyte.Hypsibius arcticus (Murray) (Tardigrada) reached a maximum density of 470 individuals per g wet weight of algal mat and individuals took about three months to reach full size. A new species ofIsohypsibius was recorded and will be described elsewhere. Tardigrades overwintered in their cryptobiotic state. The population density of bdelloid rotifers changed cyclically, peaking at three-weekly intervals during summer. They also overwintered in their cryptobiotic state.Monogonont rotifers appeared only in summer and species succession occurred. They are thought to overwinter as resting eggs. Two bdelloid rotifers,Macrotrachela quadricornifera (Milne) andMniobia russeola (Zelinka) and one monogonont rotiferPtygura sp., are new records for continental Antarctica.     

蛭态轮虫中国新记录种及其研究展望

轮虫动物门蛭态亚纲轮虫由于其严格的孤雌生殖和低湿休眠特性而成为吸引各领域学者研究的重要类群。研究对2018年在珠海万山群岛采集的苔藓样品进行观察,发现蛭态轮虫中国新记录种环颈敖突轮虫Otostephanos torquatus Bryce, 1913。目前国内缺少对该蛭态轮虫的详细形态描述,文章通过对该种的形态观察以及咀嚼器扫描电镜拍摄,阐述环颈敖突轮虫的主要分类特征。该物种重要分类依据为内腔里含有食物泡,轮盘带有特殊环状结构,上唇裂片呈三角形及裂片高度低于头冠高度,咀嚼器齿式7/7。通过检测该轮虫的COⅠ序列,与基因库中已有同科同属相似种的COⅠ基因序列聚类对比,证明了该种属于敖突轮属的遗传位置。相较于其他国家对蛭态轮虫的研究成果及其在进化研究中的重要地位,我国学者应该加强对蛭态轮虫的研究探索。     

Survey of moss-dwelling bdelloid rotifers from middle Arctic Spitsbergen (Svalbard)

A survey of bdelloid rotifers from moss and lichen samples collected in the middle Arctic tundra subzone of Spitsbergen (Svalbard) revealed an unexpected high species richness of 52 taxa, of which 18 fully identified species are new for the region. About one-fifth of the European bdelloid species are present. Moisture regime and geographic localization of the moss appeared the most important ecological features driving differences in species composition between samples.     

Macrotrachela quadricornifera featured in a space experiment

Macrotrachela quadricornifera, a bdelloid rotifer, is the animal model of an experiment scheduled on the International Space Station (ISS). The focus of the experiment is the role of the cytoskeleton during oogenesis and early development. Bdelloids will fly desiccated, be rehydrated on the ISS and cultivated for five generations. We present the outline of the ISS experiment, the expectations and the state-of-the-art of ground-based research run to date on the major topics of the planned experiment: anhydrobiosis and embryogenesis. Anhydrobiosis focuses on two major aspects, storage conditions that enhance recovery rate and comparison of the resistance between dormant and active rotifers to UV radiation and other environmental injuries. Embryogenesis has been approached at the morphological level under ground conditions: developing embryos have been studied by light and confocal microscopes.     

Testing for evidence of inefficient selection in bdelloid rotifers: do sample size and habitat differences matter?

Preliminary evidence on inefficient selection has indicated that asexual (=parthenogenetic) animals suffer from a greater accumulation of deleterious mutations compared with their closest sexual sister taxa. However, previous work on bdelloid rotifers did not completely rule out the confounding effects of sample size and habitat differences. Here, we present further evidence of inefficient selection against deleterious mutations in the bdelloid rotifers in comparison with their closest clade, the monogononts, by taking account of larger samples. However, the analysis of samples from both clades co-occurring in the same location seems to contradict the hypothesis. Both groups show evidence of the accumulation of deleterious mutations in mitochondrial DNA, but further population sampling and inclusion of additional genes is needed to resolve this issue.     

Bdelloid rotifers: ‘sleeping beauties’ and ‘evolutionary scandals’, but not only

Bdelloid rotifers are mostly known for two peculiarities, continuous parthenogenetic reproduction and dormancy in response to habitat desiccation, a phenomenon named anhydrobiosis. These uncommon traits earned them the names of ‘evolutionary scandals’ and ‘sleeping beauties’, respectively. Relevant aspects of bdelloid biology have recently been described that connect parthenogenesis to anhydrobiosis and that might account for their evolutionary survival in spite of the conservative reproduction. In the present study, I explore recent literature, in the attempt to disentangle the apparent incongruency between the apomictic reproduction and the presumed long-term evolutionary survival of bdelloid species. Recent results remarkably improved our knowledge of bdelloid population biology, genetics, and molecular biology. The most relevant findings concern (i) acquisition of foreign genes through horizontal transfer, (ii) presence of divergent sequences possibly corresponding to ancient gene duplications and (iii) capacity to escape parasites: events that appear to be connected with dormancy. I also address the results of recent studies on the relationships between bdelloids and other rotifers, including acanthocephalans, in an attempt to highlight similarities and differences that should be clarified to better understand phylogenetic relationship among the Rotifera sensu lato.

     

A carnivorous bdelloid rotifer, Abrochtha carnivora n.sp.

Abstract. Here we describe a new bdelloid rotifer, Abrochtha carnivora n.sp., that preys on other bdelloids and monogonont rotifers. This is the first report of predatory behavior in bdelloids. Despite this extraordinary behavior, A. carnivora displays no major structural deviation from the standard body plan for members of the bdelloid family Philodinavidae: body with head (with ciliated corona), trunk, and foot, mastax with ramate trophi. The finding of such a carnivorous species, unique for the class, appears to contradict the common assumption that the wholly parthenogenetic bdelloids are evolutionary dead-ends.     

Recipes for successful anhydrobiosis in bdelloid rotifers

We tested the effect of several environmental variables on the ability of three bdelloid rotifers (Macrotrachela quadricornifera, Philodina roseola and Adineta oculata) to recover from the anhydrobiotic state. The variables we examined were (1) rate of water evaporation, (2) relative humidity during anhydrobiosis, (3) temperature during anhydrobiosis, (4) duration of anhydrobiosis, and (5) rehydration rate. Our results indicate that bdelloids can regulate to some degree net water balance during onset and termination of anhydrobiosis.     

A survey of introns in three genes of rotifers

Here we report on the occurrence and position of introns found in three genes of rotifers. A region of the gene for the TATA-box binding protein was examined in three species of Bdelloidea and one of Monogononta. There are two introns in both copies of this gene present in each of the three bdelloids examined – one at a position where introns occur in other eukaryotes and the other at a novel position; the monogonont has no introns in the region examined. A region of the gene encoding the 82 kD heat shock protein was examined in 10 species, with every rotifer class represented. Introns were found in only two species, both bdelloids: one of the species has an intron in all three copies of the gene; the other has an intron in only one of the three copies. Both introns occur at novel positions. The gene for triosephosphate isomerase was examined in one bdelloid. Both copies of the gene in this species contain introns, all at conserved positions: one copy contains five introns, the other copy three. These observations demonstrate the presence of introns in bdelloid rotifers, some in conserved positions, others apparently newly arisen during bdelloid evolution.     

Weak swimming response of a bdelloid rotifer to chemical cues of a native copepod predator

Journal of Ethology - Whether bdelloid rotifers can detect and respond to the chemical cues of predators has not been studied, and research on their behaviour is scarce in general. To test for such...     

Bdelloid rotifers and nematodes in a small Italian stream

SUMMARY. The bdelloid rotifers and nematodes of a small clean watercourse in the area surrounding the Po river near Parma have been studied. The samples were collected at two sites 400 m apart. The species found in twelve collections of benthos between May 1977 and June 1978 were eighteen belonging to Bdelloidea and forty-seven to Nematoda (Tylenchida have not been considered). Nearly all the bdelloid species were oligosaprobic or beta-mesosaprobic; the Shannon index of diversity was 3.0 at the first site and 2.4 at the second. Among the Nematoda the dominant species were Paraplectonema pedunculatum and Paraphanolaimus anisitsi which were not previously recorded for Italy. Nearly all nematodes are microphagous; predators represent only 10% of collected specimens. Polluted water indicator species (Secernentia group) were only 3.5% of the total nematodes recorded. Most rotifers and nematodes did not show seasonal fluctuations in numbers. The two sampling sites do not seem to have substantial differences in the taxocoenosis of Rotifera and Nematoda; their percentage of similarity is 69% and 79% for the two classes respectively.     

Genomic clues to an ancient asexual scandal

Despite abandoning meiosis, the bdelloid rotifers have persisted for millions of years and given rise to hundreds of species. Several mechanisms - allelic variants with different functions, high effective population size, and resistance to radiation - may contribute to their success.