Spatial and temporal escape from fungal parasitism in natural communities of anciently asexual bdelloid rotifers

Sexual reproduction is costly, but it is nearly ubiquitous among plants and animals, whereas obligately asexual taxa are rare and almost always short-lived. The Red Queen hypothesis proposes that sex overcomes its costs by enabling organisms to keep pace with coevolving parasites and pathogens. If so, the few cases of stable long-term asexuality ought to be found in groups whose coevolutionary interactions with parasites are unusually weak. In theory, antagonistic coevolution will be attenuated if hosts disperse among patches within a metapopulation separately from parasites and more rapidly. We examined whether these conditions are met in natural communities of bdelloid rotifers, one of the longest-lived asexual lineages. At any life stage, these microscopic invertebrates can tolerate the complete desiccation of their ephemeral freshwater habitats, surviving as dormant propagules that are readily carried by the wind. In our field experiments, desiccation and wind transport enabled bdelloids to disperse independently of multiple fungal parasites, in both time and space. Surveys of bdelloid communities in unmanipulated moss patches confirmed that fungal parasitism was negatively correlated with extended drought and increasing height (exposure to wind). Bdelloid ecology therefore matches a key condition of models in which asexuals persist through spatio-temporal decoupling from coevolving enemies.     

Evidence for inefficient selection against deleterious mutations in cytochrome oxidase I of asexual bdelloid rotifers

Evolutionary theory predicts that natural selection should be less efficient in asexually than in sexually reproducing organisms. Obligate asexuals are expected to adapt slowly to changing environments and to accumulate mildly deleterious mutations to their genomes, potentially explaining their typically short evolutionary lifespans. One group of animals that appear to challenge these ideas is the bdelloid rotifers, a large and ancient clade of obligate asexuals. Previous work has found no evidence for inefficient selection against deleterious mutations in protein-coding genes of bdelloids. However, these studies relied mostly on between-species comparisons and were therefore unable to detect mildly deleterious mutations that persist within populations but are removed by selection over longer time periods. Here, we test for inefficient purifying selection acting on the cytochrome oxidase I (cox1) mitochondrial gene in 3 clades of bdelloids. Patterns of variation are compared to those of two facultatively sexual clades: a monogonont rotifer (Brachionus) and a branchiopod crustacean (Daphnia). As predicted due to the strict linkage between mitochondrial and nuclear genomes, bdelloids exhibit higher frequencies of putatively deleterious amino acid polymorphism within populations than the two facultatively sexual clades. While the monophyly and age of bdelloids makes it hard to rule out other explanations for the observed differences, several possible confounding factors, such as differences in effective population size or patterns of codon usage, are shown not to explain the observed differences. We therefore conclude that bdelloid mitochondrial DNA variation does display the signature of inefficient selection expected of obligate asexuals.     

Inconsistent estimates of diversity between traditional and DNA taxonomy in bdelloid rotifers

Microscopic animals offer great potential in the analysis of spatial patterns of diversity, as they may provide different scenarios for biogeography and macroecology, but understanding diversity of microscopic animals is hampered by lack of comprehensive data on species distribution and by unreliable taxonomy. DNA taxonomy may prove useful in obtaining reliable data in the future, but we still do not know to what extent traditional and DNA taxonomy can be comparable for microscopic organisms. In this paper, we compare analyses and estimates of diversity at the level of species assemblage between traditional and DNA taxonomy for a group of moss-dwelling microscopic animals, bdelloid rotifers. The results are straightforward: Traditional species identification underestimates diversity by factors of 2 at the local and 2.5 at the regional scale. We discuss the results in the framework of current hypotheses on the distribution of microscopic animals.     

A quantitative analysis of the Eutherian orbit: correlations with masticatory apparatus

The mammalian orbit, or eye-socket, is a highly plastic region of the skull. It comprises between seven and nine bones, all of which vary widely in their contribution to this region among the different mammalian orders and families. It is hypothesised that the structure of the mammalian orbit is principally influenced by the forces generated by the jaw-closing musculature. In order to quantify the orbit, fourteen linear, angular and area measurements were taken from 84 species of placental mammals using a Microscribe-3D digitiser. The results were then analysed using principal components analysis. The results of the multivariate analysis on untransformed data showed a clear division of the mammalian taxa into temporalis-dominant forms and masseter-dominant forms. This correlation between orbital structure and masticatory musculature was reinforced by results from the size-corrected data, which showed a separation of the taxa into the three specialised feeding types proposed by Turnbull (1970): i.e. 'carnivore-shear', 'ungulate-grinding' and 'rodent-gnawing'. Moreover, within the rodents there was a clear distinction between species in which the masseter is highly developed and those in which the temporalis has more prominence. These results were reinforced by analysis of variance which showed significant differences in the relative orbital areas of certain bones between temporalis-dominant and masseter-dominant taxa. Subsequent cluster analysis suggested that most of the variables could be grouped into three assemblages: those associated with the length of the rostrum; those associated with the width of the skull; and those associated with the relative size of the orbit and the shape of the face. However, the relative area of the palatine bone showed weak correlations with the other variables and did not fit into any group. Overall the relative area of the palatine was most closely correlated with feeding type, and this measure that appeared to be most strongly associated with the arrangement of the masticatory musculature. These results give a strong indication that, although orbital structure is in part determined by the relative size and orientation of the orbits, the forces generated by the muscles of mastication also have a large effect.     

中国蛭态轮虫亚纲6种新记录种记述

轮虫是浮游动物的重要组成部分,蛭态轮虫作为轮虫动物门的重要类群,因其孤雌生殖、低湿休眠和水平基因转移的特性成为国际上的研究热点。蛭态轮虫物种的形态学鉴定是进行其生态学、分子生物学和基因工程研究的基础,具有重要意义。本研究以广东白云山和火炉山为调查区域,共发现蛭态轮虫中国新记录科1科,即原轮科（Philodinavidae Harring,1913）,新记录属2属,即原盘轮属（Henoceros Milne,1916）和双趾轮属（Didymodactylos Milne,1916）,以及新记录种6种,包括有尾原盘轮虫[H. caudatus（Hauer,1937）]、巨趾原盘轮虫[H. falcatus（Milne,1916）]、多肉双趾轮虫[D. carnosus（Milne,1916）]、皇家敖突轮虫[Otostephanos regalis（Milne,1916）]、圆腹粗颈轮虫[Macrotrachela kallosoma（Schulte,1954）]以及长肌宿轮虫[Habrotrocha longiceps（Murray,1906）]。通过显微照片和模式图详细记述了新记录种的形态结构特征。本研究丰富了我国蛭态轮虫的物种记录,同时也为后续应用研究提供基础资料和分类参考。     

genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms

Investigating diversity in asexual organisms using molecular markers involves the assignment of individuals to clonal lineages and the subsequent analysis of clonal diversity. Assignment is possible using a distance matrix in combination with a user‐specified threshold, defined as the maximum distance between two individuals that are considered to belong to the same clonal lineage. Analysis of clonal diversity requires tests for differences in diversity and clonal composition between populations. We developed two programs, genotype and genodive for such analyses of clonal diversity in asexually reproducing organisms. Additionally, genotype can be used for detecting genotyping errors in studies of sexual organisms.     

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.     

Interspecific analysis of covariance structure in the masticatory apparatus of galagos

The primate masticatory apparatus (MA) is a functionally integrated set of features, each of which performs important functions in biting, ingestive, and chewing behaviors. A comparison of morphological covariance structure among species for these MA features will help us to further understand the evolutionary history of this region. In this exploratory analysis, the covariance structure of the MA is compared across seven galago species to investigate 1) whether there are differences in covariance structure in this region, and 2) if so, how has this covariation changed with respect to size, MA form, diet, and/or phylogeny? Ten measurements of the MA functionally related to bite force production and load resistance were obtained from 218 adults of seven galago species. Correlation matrices were generated for these 10 dimensions and compared among species via matrix correlations and Mantel tests. Subsequently, pairwise covariance disparity in the MA was estimated as a measure of difference in covariance structure between species. Covariance disparity estimates were correlated with pairwise distances related to differences in body size, MA size and shape, genetic distance (based on cytochrome‐b sequences) and percentage of dietary foods to determine whether one or more of these factors is linked to differences in covariance structure. Galagos differ in MA covariance structure. Body size appears to be a major factor correlated with differences in covariance structure among galagos. The largest galago species, Otolemur crassicaudatus, exhibits large differences in body mass and covariance structure relative to other galagos, and thus plays a primary role in creating this association. MA size and shape do not correlate with covariance structure when body mass is held constant. Diet also shows no association. Genetic distance is significantly negatively correlated with covariance disparity when body mass is held constant, but this correlation appears to be a function of the small body size and large genetic distance for Galagoides demidoff. These exploratory results indicate that changing body size may have been a key factor in the evolution of the galago MA. Am. J. Primatol. 69:46–58, 2007. © 2006 Wiley‐Liss, Inc.     

Potential niche displacement in species of aquatic bdelloid rotifers between temperate and tropical areas

Hydrobiologia - Bdelloids are commonly found in freshwaters or limno-terrestrial habitats. No formal attempt has yet been performed to define bdelloid niche and to identify whether species respond...     

Feeding and anhydrobiosis in bdelloid rotifers: a preparatory study for an experiment aboard the International Space Station

Abstract. Here we report the effect of food concentration on the recovery from anhydrobiosis of a bdelloid rotifer, Macrotrachela quadricornifera . Cohorts were either starved, or fed high or low concentrations of food, before being dried and their subsequent recovery rates determined. The rotifers starved for 3 d before anhydrobiosis recovered in significantly higher proportion, and those fed lower food concentration recovered better than those fed higher food concentration. In addition, starvation did not decrease the recovery of other bdelloid species ( Philodina roseola and Adineta sp. 1) which were either fed or starved before anhydrobiosis. These results suggest that a successful recovery from anhydrobiosis is not dependent on prior resource level supplied to the bdelloids. However, the lack of resources might not be the only factor in a successful recovery from anhydrobiosis. Observations using scanning electron microscopy of fed individuals of M. quadricornifera entering anhydrobiosis showed that some food remained in the digestive tract. Thus, we propose that the negative effect of rich food may be due to a purely mechanical effect and may be interfering with a proper folding of the rotifer body at the onset of anhydrobiosis. This contribution results from studies carried out in preparation for biological experiments scheduled on the International Space Station (ISS).     

Supraorbital ridge and masticatory apparatus I: Primates

The supraorbital ridge formation in apes is a result of the traction of the masticatory force exerted by the anterior part of the temporalis muscle. This force varies inversely with the ratio of the power arm to the load arm of the mandible. The smaller this ratio, the greater the anterior part of the temporalis muscle and the larger the supraorbital ridge. The size of the ridge is independent of the actual size of the skull. The orang has a larger skull but the smallest brow ridge of the three species studied: gorilla, chimpanzee and orang. Pearson’s correlation coefficient shows a positive correlation between the anterior temporalis muscle and the ridge as well as between the ridge/sinus and anterior/whole temporalis muscle. The correlation is negative between the power/load arms and anterior/whole muscle and also between the power/load arms and the ridge/sinus ratio.     

Musculature of two bdelloid rotifers, Adineta ricciae and Macrotrachela quadricornifera: organization in a functional and evolutionary perspective

Organization of muscles in microinvertebrates has often been studied to answer functional questions and understand phylogenetic relationships among taxa. In this study, the musculature of two bdelloid species, Adineta ricciae and Macrotrachela quadricornifera , was illustrated, and their organization was compared with other rotifer taxa to generate possible hypotheses of evolutionary relationships among Rotifera. The two species share a common habitat but differ from each other in feeding and locomotion. A. ricciae feeds on the biofilm by scraping it, is unable to swim, and slides on the head cilia using the foot to propel over the substratum. M. quadricornifera feeds by filtration, can swim, and advances by looping in a leech-like motion. Their musculature, stained with TRITC-phalloidin, was observed using confocal laser scanning microscopy. Major differences between the two species were observed in the muscles of head and foot, possibly reflecting differences in their life style. Muscles of the trunk were similarly arranged: circular muscles surrounded longitudinal bands, which were inserted at different points on the body wall. In both bdelloids, circular muscles of the trunk were incomplete ventrally, a condition also present in Seison and in soft-bodied monogononts from benthos. Within rotifers, circular muscles in the form of complete rings are present in acanthocephalans and in soft-bodied planktonic monogononts but are absent in loricate monogononts, which generally possess dorsoventral bands. The diversity of muscle organization among rotifers was interpreted and discussed.     

Supraorbital ridge and masticatory apparatus II: Humans (Eskimos)

Thirteen adult male skulls of St. Lawrence Island Eskimos were studied to determine the factor or factors responsible for the development of the supraorbital ridges. Results showed that the determining factor is the ratio of the power arm to the load arm of the mandible. The smaller this ratio, the greater the traction force exerted by the anterior temporalis muscle and the greater the supraorbital ridge. Pearson’s correlation coefficient shows two positive correlations, i.e. between the anterior temporalis muscle and the ridge and between the ridge/sinus and the anterior/whole temporalis muscle. Conversely, there is a negative correlation between the power/load arm and the muscle ratio as well as between the power/load arm ratio and the ridge/sinus ratio.     

Ultrastructure of the asexual apparatus in Mycotypha (Mucorales)

The development of the asexual apparatus of Mycotypha africana and Mycotypha poitrasii observed by means of scanning electron microscopy is reported. Using ultrathin sections and freeze-fracture replicas, sporangiole structure is described. Sporangiospore structure is compared with that of other members of the Thamnidiaceae.     

Planktonic and periphytic bdelloid rotifers from Thailand reveal a species assemblage with a combination of cosmopolitan and tropical species

The dispersal pattern of microorganisms has been a debated topic in the last decade, because for microscopic organisms with dispersing stages, biogeographic barriers may not exist and geographic distances may have little effect on the probability of their occurrence. In this study we tested whether a group of microscopic animals, the bdelloid rotifers, sampled in a tropical country, could indeed be cosmopolitan, strictly tropical, and/or have endemic species. We sampled freshwater habitats throughout Thailand in dry and rainy seasons between 2014 and 2016, focusing on permanent water bodies, where the prevalence of species producing resting stages acting as propagules for dispersal should be minimal and thus dispersal limitation should exist, with several species being narrowly distributed. We used traditional morphological identification, geometric morphometric analyses on the shape and size of the jaws, and DNA taxonomy to identify species and to quantify the morphological and genetic distances of Thai samples in comparison with data on bdelloids from other areas in the world. We found a total of 12 species of planktonic and periphytic bdelloid rotifers, and all approaches we used, qualitative and quantitative, confirmed a group of nine potentially cosmopolitan species already known from other continents, one tropical oriental species, and two new species with a potentially narrow geographic distribution, one of which we here formally describe. We thus support the idea that for microscopic animals the moderate endemicity hypothesis suggested for protists may also hold true: most of the species we found indeed have a wide geographic distribution, but other species with narrower distributions do exist.

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