Anciently Asexual Bdelloid Rotifers Escape Lethal Fungal Parasites by Drying Up and Blowing Away

Wilson, Christopher G.; Sherman, Paul W.

doi:10.1126/science.1179252

Cited by 65 publications

(58 citation statements)

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“…The most commonly recorded enemies of bdelloid rotifers are lethal fungal and oomycete parasites (ca 50 species: [37]), chiefly belonging to the genus Rotiferophthora, which preys specifically upon them. It has been demonstrated experimentally that Rotiferophthora angustispora cannot withstand desiccation or disperse by wind to the same degree as its bdelloid host, Habrotrocha elusa [26]. Desiccation for 35 days eliminated the fungus from over 90% of cultured rotifer populations, and when infected cultures were desiccated for just 7 days, but also subjected to dispersal in a wind chamber, the prevalence of parasites in newly founded populations was reduced by 60% relative to water-dispersed controls.…”

Section: Introductionmentioning

confidence: 99%

“…However, it has been suggested that bdelloid rotifers may fit the requirements [22,26,27]. They are found in almost every freshwater and limno-terrestrial habitat patch worldwide, however tiny, remote or ephemeral.…”

Section: Introductionmentioning

confidence: 99%

“…It has been suggested that the physically and physiologically stressful processes of extended anhydrobiotic dormancy and dispersal by wind could separate bdelloid rotifers from their parasites in both time and space [22,26,27]. If rotifers survive desiccation better than their enemies, an episode of drought could purge coadapted parasites from a habitat patch, and store host genotypes in a temporal 'bank' of tuns, to be recycled against different parasites in future wet periods.…”

Section: Introductionmentioning

confidence: 99%

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

Wilson

Sherman

2013

Proc. R. Soc. B.

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Sexual reproduction is costly, but it is nearly ubiquitous among plants and animals, whereas obligately asexual taxa are rare and almost always shortlived. 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.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Wilson

Sherman

2013

Proc. R. Soc. B.

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“…Nevertheless, it remains to be determined how often parasites elicit a coevolutionary arms race that is resolved by the host engaging in high rates of sex, or whether it is resolved by alternative mechanisms (e.g., ref. 17). Another empirical challenge is to get a better estimate of the real costs of sex across the many eukaryotic lineages.…”

Section: Discussionmentioning

confidence: 99%

“…"Ancient asexuals" are hypothesized to possess the traits to deal with such long-term challenges. Bdelloid rotifers, one of the best examples of ancient asexuality, show some characteristics that might be interpreted as alternative forms of genetic exchange (14,15), exceptional DNA repair mechanisms (16), and nongenetic means of evading fungal parasites (17).…”

Section: Asexual Invasionsmentioning

confidence: 99%

Does the avoidance of sexual costs increase fitness in asexual invaders?

Stelzer

2015

Proc. Natl. Acad. Sci. U.S.A.

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The high prevalence of sexual reproduction is considered a paradox mainly for two reasons. First, asexuals should enjoy various growth benefits because they seemingly rid themselves of the many inefficiencies of sexual reproduction-the so-called costs of sex. Second, there seems to be no lack of asexual origins because losses of sexual reproduction have been described in almost every larger eukaryotic taxon. Current attempts to resolve this paradox concentrate on a few hypotheses that provide universal benefits that would compensate for these costs and give sexual reproduction a net advantage. However, are new asexual lineages really those powerful invaders that could quickly displace their sexual ancestors? Research on the costs of sex indicates that sex is often stabilized by highly lineage-specific mechanisms. Two main categories can be distinguished. First are beneficial traits that evolved within a particular species and became tightly associated with sex (e.g., a mating system that involves sexual selection, or a sexual diapausing stage that allows survival through harsh periods). If such traits are absent in asexuals, simple growth efficiency considerations will not capture the fitness benefits gained by skipping sexual reproduction. Second, lineage-specific factors might prevent asexuals from reaching their full potential (e.g., dependence on fertilization in spermdependent parthenogens). Such observations suggest that the costs of sex are highly variable and often lower than theoretical considerations suggest. This has implications for the magnitude of universal benefits required to resolve the paradox of sex. evolution of sex | genetic variation | mating systems | clonality | parthenogenesis

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Rotifera

Wallace

Smith

2013

Encyclopedia of Life Sciences

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Rotifera is a moderately sized phylum of minute, bilaterally symmetrical, unsegmented animals that live predominantly in freshwaters. The phylum name (Latin, rota , wheel; ferre , to bear), first used by Cuvier in 1798, refers to the anterior end that in many species resembles a rotating wheel due to the sequential beat of its cilia. Rotifers have been found on every continent, occupying a diverse array of habitats, including marine, brackish and freshwaters, as well as the film of water that coats terrestrial mosses and particles in damp soils. In lakes rotifers often achieve high population densities (>1000 individuals per litre); thus, as consumers of bacteria, algae and protists they are ecologically important in transferring energy to higher trophic levels. As rotifers are a good food for young fishes, they are grown in mass quantities in commercial aquaculture. They also serve as models for research on ageing, and as bioindicators for ecotoxicology. Key Concepts: Rotifers have been found in the inland waters (both fresh and saline) of every continent, in the moisture covering some plants such as mosses, and in damp soil. Although generally not as abundant as in continental waters, rotifers often flourish in nearshore marine waters and estuaries. Many rotifers are capable of undergoing dormancy, either as adults or embryos, allowing them to disperse in space or time and often avoid harsh conditions. Feeding mainly on other microscopic organisms, including bacteria, algae and protists, rotifers are important basal consumers in aquatic systems. In certain lakes, rotifers play an important role connecting the microbial loop to the classic food web, whereby the dissolved organic carbon is taken up by the bacteria that are consumed by rotifers, which in turn are consumed by higher trophic levels. In this way, a portion of the energy in dissolved organic matter is returned to the food web. As they are the first food for larval organisms, rotifers have been exploited by aquaculturists to maintain commercially important fishes, shrimps and crabs. As they are comparatively inexpensive and easy to culture and possess relatively short life spans, rotifers are used in ageing studies and to assess the toxicity of compounds such as heavy metals, pesticides and pharmaceuticals. Some species of rotifers have specific ecological requirements making them useful as indicators of water quality. The phylogenetic position of rotifers has not yet been resolved, but they appear to be related to a group of small, jawed metazoans (Gnathifera). Acanthocephala, an entirely parasitic phylum, are now considered to be highly aberrant rotifers. Over the years rotifers have entered the collective culture ethos as subjects of poetry, science fiction and children's literature, artists' workings in glass and mixed media and pop music.

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Anciently Asexual Bdelloid Rotifers Escape Lethal Fungal Parasites by Drying Up and Blowing Away

Cited by 65 publications

References 19 publications

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

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

Does the avoidance of sexual costs increase fitness in asexual invaders?

Rotifera

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