On choice of substrate and habitat in bdelzoid rotifers

Information on the distributions of 77 bdelloid rotifers from diverse waters in south and central Sweden was analyzed to reveal their relationships to substrate and habitat. Only two species were reported from plankton, both in low frequency. An artificial substrate, white cotton, was utilized only by few bdelloids, mainly by species with eyes. Only one species occurred at higher frequency on the saprobic substrate Sphaerotilus. Most bdelloids prefer environments rich in oxygen, but some species may be found in soft-bottom sediments. Several species dwell preferentially in diverse habitats of bogs. Some bdelloids have an exceptionally broad ecological range, but even for these is it possible to distinguish a pattern of preference and avoidance.     

Spatial gradients in species diversity of microscopic animals: the case of bdelloid rotifers at high altitude

Aim Organisms smaller than 2 mm appear not to follow the spatial patterns in richness and diversity commonly observed in macroscopic organisms. We describe spatial patterns in species diversity in a group of microscopic organisms, bdelloid rotifers, living in moss and lichen patches, in order to test the hypotheses of no relationship between species richness and composition and spatial gradients, suggested by previously published patterns in microscopic organisms. Location Moss and lichen patches as habitats for bdelloids, on high‐elevation peaks at altitudes between 2984 and 4527 m a.s.l. across the Italian, French and Swiss Alps, with distances among sample sites ranging from 1 m to 420 km, in comparison with lower‐elevation samples at altitudes from 850 to 1810 m a.s.l. Methods We sampled species assemblages of bdelloid rotifers living in isolated moss and lichen patches in 47 sites. We described the observed α, β and γ diversities; the heterogeneity of species assemblages; and the estimated number of species (incidence‐based coverage estimator). Patterns in species distribution were analysed at three different levels: (1) habitat, comparing species richness on moss and lichen substrates, testing differences in α diversity and heterogeneity (anova ), species composition (analysis of similarities test), and γ diversity (rarefaction curves); (2) altitude, comparing the observed richness with previously published data from locations well below 2000 m; and (3) distances between sites, correlating the matrix of Jaccard dissimilarities and the matrix of geographical distances with a Mantel test. Results Both species richness and species composition of bdelloid rotifers differed significantly between mosses and lichens at high elevations, but no difference was found in the heterogeneity of species assemblages. Alpha diversity was significantly lower at high‐elevation than at low‐elevation sites, but the estimated number of species was not reduced when compared with sites at low elevations. Geographical distance between sites had no effect on species composition in either mosses or lichens. The distribution of species was highly heterogeneous, with a low similarity among assemblages. Main conclusions As expected, bdelloids appear to occupy habitats selectively. The altitudinal gradient in species richness for bdelloid rotifers is limited to a decrease in α diversity only; such a decrease is not caused by a lower number of species (low γ diversity) being able to tolerate harsh conditions, and high‐altitude species are not a subset of species living at lower elevations. The observed values of α, β and γ diversity at high altitudes in the Alps are compatible with the scenario of a very low number of available propagules because of the low density of patches of favourable habitat. Our results suggest that the geographical distribution of animals, and therefore biodiversity patterns, may be strongly influenced by animal size, as small organisms such as bdelloids appear to show spatial patterns that differ from those known in larger animals. Differences in body size should be taken into account carefully in future studies of biodiversity patterns.     

Demographic processes underlying fitness restoration in bdelloid rotifers emerging from dehydration

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Bdelloid Rotifers from Lakes above 1700 m in Western Italian Alps,with Taxonomic Notes on Dissotrocha macrostyla

Benthic and periphytic bdelloid communities from 16 alpine lakes from 1700 to 2850 m above sea level in Sesia Valley (Piedmont region, North‐western Italy), sampled during summer 2001 and 2002, were analyzed. Seventeen species were identified from these species‐poor communities, with 1 to 6 species each. Dissotrocha macrostyla and Philodina citrina were the most common species, present in 10 lakes while 9 species were collected from one lake only. New morphological details from S.E.M. pictures of Dissotrocha macrostyla revealed that Dissotrocha macrostyla tuberculata (Gosse , 1886) is only a seasonal morphotype. Its different appearance is due to the presence of locally distributed microscopic mucous bubbles (diameter 1.41 ± 0.18 μm) on the trunk surface, produced by the rotifer itself under stressful conditions.     

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.     

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.     

Cryptic diversity in the genus <Emphasis Type="Italic">Adineta</Emphasis> Hudson &; Gosse, 1886 (Rotifera: Bdelloidea: Adinetidae): a DNA taxonomy approach

Cryptic species are continuously discovered in rotifers using different methods to delineate these units of diversity. DNA taxonomy is the most effective method taxonomists have to untie potential cryptic taxa. Here, we estimate hidden diversity in a genus of bdelloid rotifers, Adineta. We analyse cryptic diversity using a coalescent approach to infer evolutionarily significant units from a phylogenetic tree obtained from cytochrome oxidase I sequences. Cryptic diversity was measured for eight traditional species and from several additional undetermined populations. Taxonomic inflation of up to 36 taxa was found in A. vaga from DNA taxonomy. As observed in other microscopic organisms, cryptic taxa within each traditional species were not geographically isolated, but had significantly narrower ecological niches than expected by chance alone.     

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.     

A Putative LEA Protein,but no Trehalose,is Present in Anhydrobiotic Bdelloid Rotifers

Some eukaryotes, including bdelloid rotifer species, are able to withstand desiccation by entering a state of suspended animation. In this ametabolic condition, known as anhydrobiosis, they can remain viable for extended periods, perhaps decades, but resume normal activities on rehydration. Anhydrobiosis is thought to require accumulation of the non-reducing disaccharides trehalose (in animals and fungi) or sucrose (in plant seeds and resurrection plants), which may protect proteins and membranes by acting as water replacement molecules and vitrifying agents. However, in clone cultures of bdelloid rotifers Philodina roseola and Adineta vaga, we were unable to detect trehalose or other disaccharides in either control or dehydrating animals, as determined by gas chromatography. Indeed, trehalose synthase genes (tps) were not detected in these rotifer genomes, suggesting that bdelloids might not have the capacity to produce trehalose under any circumstances. This is in sharp contrast to other anhydrobiotic animals such as nematodes and brine shrimp cysts, where trehalose is present during desiccation. Instead, we suggest that adaptations involving proteins might be more important than those involving small biochemicals in rotifer anhydrobiosis: on dehydration, P. roseola upregulates a hydrophilic protein related to the late embryogenesis abundant (LEA) proteins associated with desiccation tolerance in plants. Since LEA-like proteins have also been implicated in the desiccation tolerance of nematodes and micro-organisms, it seems that hydrophilic protein biosynthesis represents a common element of anhydrobiosis across several biological kingdoms.     

Stress and fitness in parthenogens: is dormancy a key feature for bdelloid rotifers?

Background

Bdelloid rotifers are the most common and abundant group of animals that reproduce by ameiotic parthenogenesis, only. They are common in temporally ephemeral habitats, and it is unclear if they dwell in unstable habitats because are excluded from better conditions by stronger competitors, or because they need unstable conditions for their success. We tested the hypothesis that bdelloids 'require' stressful conditions for their persistence by comparing fitness-related traits of stressed (desiccated, D) and unstressed (hydrated, H) lines of two species, Adineta ricciae and Macrotrachela quadricornifera.

Results

For both bdelloid species, fecundity was significantly lower in H than in parallel D line. Fitness components decreased with time progressively in the H line but not in the D line. Recovery rates of D lines were recorded after every desiccation and did not reveal any trend in time, suggesting that no selection was operating.

Conclusion

Stress in the form of reiterated desiccations seemed to help both bdelloid species to keep fitness stable; in contrast under stable conditions, like permanent hydration, these bdelloid species had poorer performances. Bdelloids, although aquatic animals, are not only efficient in tolerating desiccation, but seem somehow dependent on anhydrobiosis, a circumstance that might represent a key event in their life cycle. If this is true, life in unpredictable habitats should not be seen as the result of competitive exclusion from 'easier' habitats, but a requirement for long-term survival of these parthenogenetic animals.

     

Swimming speed and Reynolds numbers of eleven freshwater rotifer species

We obtained data on the swimming speed of 11 freshwater rotifer species. These data were analyzed in terms of Reynolds numbers given the fact that rotifers are in the evolutionary boundary between the use of cilia and swimming appendages. Swimming speed ranged from 0.174 to 0.542 mm ^–1. Philodina acuticornis odiosa was the fastest rotifer in terms of absolute speed. However, Gastropus hyptopus, the smallest of the rotifers analyzed, was the fastest (2.849) in terms of body-lengths s^–1. Reynolds numbers (Re) among the 11 species analyzed varied from 0.023 to 0.301. Lecane furcata had the smallest Re, while Epiphanes senta had the highest Re. The two bdelloid rotifers analyzed in this work swam five times faster than they crept. The importance of Reynolds numbers and drag coefficients are discussed in view of the present results and data found in the literature.     

Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy

Knowledge and estimates of species richness at all scales are biased both by our understanding of the evolutionary processes shaping diversity and by the methods used to delineate the basic units of diversity. DNA taxonomy shows that diversity may be underestimated by traditional taxonomy, especially for microscopic animals. The effects of such hidden diversity are usually overlooked in ecological studies. Here, we estimate hidden diversity in bdelloid rotifers, a group of microscopic animals. We analyse cryptic diversity using a coalescent approach to infer taxonomical units from phylogenetic trees. Cryptic diversity was measured for eight traditional species of bdelloid rotifers and the results compared to that of the monogonont rotifer Brachionus plicatilis species complex, which is well studied and for which cross-mating experiments have been performed to explicitly define some of the species boundaries. A taxonomic inflation of up to 34 potential cryptic taxa was found in bdelloids. Cryptic taxa within each traditional species may be spatially isolated, but do not have narrower ecological niches. The species deemed as generalists exhibit the highest cryptic diversity. Cryptic diversity based on molecular characterization is commonly found in animals; nevertheless, the amount of cryptic diversity in bdelloids is much higher than in other groups analysed so far, maybe because of their peculiar parthenogenetic reproduction, other than microscopic size. We discuss this hypothesis in the light of the available empirical evidence from other groups of microscopic invertebrates, such as tardigrades and mites, which share size, habitat heterogeneity, potential for dispersal, and/or parthenogenetic reproduction.     

Repeated convergent evolution of parthenogenesis in Acariformes (Acari)

The existence of old species‐rich parthenogenetic taxa is a conundrum in evolutionary biology. Such taxa point to ancient parthenogenetic radiations resulting in morphologically distinct species. Ancient parthenogenetic taxa have been proposed to exist in bdelloid rotifers, darwinulid ostracods, and in several taxa of acariform mites (Acariformes, Acari), especially in oribatid mites (Oribatida, Acari). Here, we investigate the diversification of Acariformes and their ancestral mode of reproduction using 18S rRNA. Because parthenogenetic taxa tend to be more frequent in phylogenetically old taxa of Acariformes, we sequenced a wide range of members of this taxon, including early‐derivative taxa of Prostigmata, Astigmata, Endeostigmata, and Oribatida. Ancestral character state reconstruction indicated that (a) Acariformes as well as Oribatida evolved from a sexual ancestor, (b) the primary mode of reproduction during evolution of Acariformes was sexual; however, species‐rich parthenogenetic taxa radiated independently at least four times (in Brachychthonioidea (Oribatida), Enarthronota (Oribatida), and twice in Nothrina (Oribatida), (c) parthenogenesis additionally evolved frequently in species‐poor taxa, for example, Tectocepheus, Oppiella, Rostrozetes, Limnozetes, and Atropacarus, and (d) sexual reproduction likely re‐evolved at least three times from species‐rich parthenogenetic clusters, in Crotonia (Nothrina), in Mesoplophora/Apoplophora (Mesoplophoridae, Enarthronota), and in Sphaerochthonius/Prototritia (Protoplophoridae, Enarthronota). We discuss possible reasons that favored the frequent diversification of parthenogenetic taxa including the continuous long‐term availability of dead organic matter resources as well as generalist feeding of species as indicated by natural variations in stable isotope ratios.     

Exceptionally well‐preserved isolated eyes from Cambrian ‘Orsten’ fossil assemblages of Sweden

Abstract: Eyes other than those of trilobites are rarely preserved in the fossil record. We describe here a set of six tiny, isolated, three‐dimensionally preserved compound eyes. These secondarily phosphatized eyes were etched from ‘Orsten’ limestone nodules dated to the Agnostus pisiformis Biozone from the Cambrian Alum Shale Formation of Sweden. The ovoid eyes arise from an elongated stalk, their surface being covered by a mosaic of regular and hexagonal‐shaped facets representing the surface of ommatidia. Facet size and pattern change within the same specimen from the posterior to the anterior end. With regard to some morphological criteria, we grouped the material in two different morphotypes, type A and B, the first being represented by specimens of two different developmental stages. From stage to stage, mostly growth in overall size and addition of new ommatidia was noticed. Among the meiobenthic ‘Orsten’ arthropods, only the crustacean Henningsmoenicaris scutula has been described as possessing stalked eyes, but the eyes of the largest specimen with preserved eyes of this species are much smaller than the new eyes and do not display any kind of ommatidia on their visual surface. However, fragments of larger specimens of H. scutula and the co‐occurrence of this species with the new isolated eyes in the sieving residues make it likely that the latter belong to this species but belong to more advanced stages than those described previously of H. scutula. Ontogenetically, the eye stalks of this fossil crustacean elongate progressively, while the regular hexagonal facets, lacking in early stages, appear later on.     

The effects of Acanthaster planci predation on populations of two species of massive coral

Species of the freshwater planarian genus Polycelis have a variable number of eyes in the head, typically more than a hundred. To elucidate the mechanisms determining the number of eyes, we investigated the relation between eye number and body length in Polycelis sapporo (Ijima & Kaburaki), a non-fissioning species, and P. auriculata Ijima & Kaburaki, a fissioning species. In P. sapporo reared at 7–8 °C, a positive correlation existed between number of eyes and body length. Eye number decreased with starvation. A similar correlation was true of P. auriculata. In specimens of P. auriculata undergoing regeneration, the rate of eye formation was higher in newly formed heads originating from larger tail-pieces than in those from smaller pieces. As a head regenerated from a tail piece or as the body size increased with feeding, the number of eyes increased. These results suggest that the number of eyes in an individual of Polycelis is determined by body length. The fine structure of the photoreceptor and pigment cells in the eyes of P. auriculata is similar to that of comparable cells in the pair of eyes in Dugesia despite the difference in the number of cells comprising an eye.     

Compound Eyes of Some Deep-Sea and Fiord Mysid Crustaceans

The compound eyes of the deep-sea mysid Boreomysis scyphops and the two mysid species Amblyops abbreviata and Pseudomma affine, which are indigenous to deep fiords in Norway, have been investigated. The eye stalks are greatly transformed, but contain hypertrophied retinas. The ommatidia of all three species lack a dioptric apparatus, possessing only retinular cells, which are arranged in a cylinder-like fashion. Folds from the retinular cells project into the “cylinder” and are covered with microvilli. The arrangement is explained functionally by an increase in the photopigment-bearing surface as an adaptation to low-light intensities. The orderly arrangement of microvilli in most arthropod compound eyes has been lost, and the arrangement is thus multidirectional in these mysids. With the photopigment dipoles arranged along the microvillar axis, the disorderly arrangement of microvilli signifies a more efficient capture of non-polarized light. It is concluded that the mysid compound eyes show adaptations to low-light intensities probably acquired during the species' evolutionary descent into deep-sea habitats. Amblyops abbreviata and Pseudomma affine, belonging to genera with entirely transformed eyes and with an ultrastructure less “normal” than that of Boreomysis scyphops are believed to be earlier descendants into the deep-sea habitats than the latter species, which belongs to a genus in which most of the species have well-developed eyes.     

Subterranean species of the ant genus Crematogaster in Asia (Hymenoptera: Formicidae)

Three Crematogaster ant species, C. (Orthocrema) javanica Menozzi, C. (O.) myops Forel and C. (O.) masukoi sp. nov., share reduced compound eyes which characterizes them among Asian species of the subgenus Orthocrema. The new species is described based on material from Borneo. It can be distinguished from C. javanica and C. myops by its smooth surface of clypeus and acutely produced subpetiolar process. Reduced compound eyes and yellowish body suggest that these three species are subterranean.