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

Wilson, Christopher G.; Sherman, Paul W.

doi:10.1098/rspb.2013.1255

Cited by 28 publications

(21 citation statements)

References 44 publications

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“…As has consistently been found in other collections of bdelloid rotifers (Birky et al 2005;Fontaneto et al 2009Fontaneto et al , 2011) the phylogeny of the mitochondrial sequences revealed distinct clades, monophyletic groups of individuals with closely related sequences well separated from other groups ( Figure 3). As found in other such bdelloid clades, there is wide geographic dispersion within clades, consistent with the minute size of bdelloids and their ability to survive desiccation and be transported by wind (Wilson and Sherman 2013).…”

Section: Resultsmentioning

confidence: 75%

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers

et al. 2015

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Rotifers of Class Bdelloidea are common freshwater invertebrates of ancient origin whose apparent asexuality has posed a challenge to the view that sexual reproduction is essential for long-term evolutionary success in eukaryotes and to hypotheses for the advantage of sex. The possibility nevertheless exists that bdelloids reproduce sexually under unknown or inadequately investigated conditions. Although certain methods of population genetics offer definitive means for detecting infrequent or atypical sex, they have not previously been applied to bdelloid rotifers. We conducted such a test with bdelloids belonging to a mitochondrial clade of Macrotrachela quadricornifera. This revealed a striking pattern of allele sharing consistent with sexual reproduction and with meiosis of an atypical sort, in which segregation occurs without requiring homologous chromosome pairs.KEYWORDS clonal erosion; cyclic parthenogenesis; meiosis; monogonont; Oenothera B DELLOID rotifers are minute freshwater invertebrates commonly found in lakes, streams, and ponds and in ephemerally aquatic environments such as rock pools and the water films on moss and lichens where they are able to survive because of their unusual ability to withstand desiccation. Although typically only several tenths of a millimeter in size, bdelloids have ganglia; muscles; reproductive, digestive, excretory, and secretory systems; photosensitive and tactile sensory organs; and structures for crawling, feeding, and swimming. Characterized by their ciliated head and bilateral ovaries and classified in four families and hundreds of morphospecies, their ancient origin is indicated by the considerable synonymous sequence divergence between families and by the finding of bdelloid remains in 35-to 40-million year old amber (Mark Welch et al. 2009).Despite much observation of field and laboratory populations and except for one heavily qualified account of having twice seen a male among many females in a sample from a lake (Wesenberg-Lund 1930), neither males, hermaphrodites, mating, nor meiosis have ever been reported within the class (Birky 2010). The only known mode of bdelloid reproduction is via eggs produced by two mitotic divisions from primary oocytes (Hsu 1956a,b). Most recently, further evidence suggestive of asexuality has come from genomic sequencing of the bdelloid Adineta vaga, showing it to be devoid of homologous chromosome pairs and therefore excluding the possibility of standard meiosis (Flot et al. 2013). Nevertheless, the possibility remains that bdelloids reproduce sexually under unknown or inadequately investigated conditions, employing a form of meiosis known in certain plants in which segregation occurs without homologous chromosome pairs-a possibility that can be tested by methods of population genetics.For any two individuals in a population descended from a common ancestor without sexual reproduction or any other sort of genetic transfer between individuals, the phylogenetic distance between a sequence in one individual and its Librar...

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Section: Resultsmentioning

confidence: 75%

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers

et al. 2015

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“…In their natural environments, such as mosses and lichens, A. vaga individuals experiencing desiccation are likely to be exposed to solar UV radiations. In some specific conditions, A. vaga can be exposed to massive UV irradiation, for instance in Arctic or Alpine mosses (Fontaneto & Melone, ; Kaya et al ., ), or when carried by wind at high altitudes (under the form of contracted ‘tun’; Wilson & Sherman, ). Besides such extreme conditions, it is interesting to outline that the relatively mild UV‐A dose used in this study was able to significantly impair A. vaga survival during desiccation.…”

Section: Discussionmentioning

confidence: 97%

Gateway to genetic exchange? DNA double‐strand breaks in the bdelloid rotifer Adineta vaga submitted to desiccation

Hespeels

Knapen

Hanot-Mambres

et al. 2014

J of Evolutionary Biology

111

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The bdelloid rotifer lineage Adineta vaga inhabits temporary habitats subjected to frequent episodes of drought. The recently published draft sequence of the genome of A. vaga revealed a peculiar genomic structure incompatible with meiosis and suggesting that DNA damage induced by desiccation may have reshaped the genomic structure of these organisms. However, the causative link between DNA damage and desiccation has never been proven to date in rotifers. To test for the hypothesis that desiccation induces DNA double-strand breaks (DSBs), we developed a protocol allowing a high survival rate of desiccated A. vaga. Using pulsed-field gel electrophoresis to monitor genomic integrity, we followed the occurrence of DSBs in dried bdelloids and observed an accumulation of these breaks with time spent in dehydrated state. These DSBs are gradually repaired upon rehydration. Even when the genome was entirely shattered into small DNA fragments by proton radiation, A. vaga individuals were able to efficiently recover from desiccation and repair a large amount of DSBs. Interestingly, when investigating the influence of UV-A and UV-B exposure on the genomic integrity of desiccated bdelloids, we observed that these natural radiations also caused important DNA DSBs, suggesting that the genome is not protected during the desiccated stage but that the repair mechanisms are extremely efficient in these intriguing organisms.

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“…How then does the Red Queen explain the existence of ancient asexual lineages? Wilson & Sherman (, ) showed that ancient asexuality may be possible in rotifers, because the rotifers can eliminate infections by entering into a desiccated resting stage. In addition, the resting stage is wind‐dispersed, independent of parasites, thus breaking the coevolutionary loop that is critical to the maintenance of sex under the Red Queen (Wilson & Sherman, , ).…”

Section: Tests Of the Red Queen Hypothesis Using Natural Populationsmentioning

confidence: 99%

The ecology of sexual reproduction

Lively

Morran

2014

J of Evolutionary Biology

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Sexual reproduction is widely regarded as one of the major unexplained phenomena in biology. Nonetheless, while a general answer may remain elusive, considerable progress has been made in the last few decades. Here we fist review the genesis of, and support for, the major ecological hypotheses for biparental sexual reproduction. We then focus on the idea that host-parasite coevolution can favor cross fertilization over uniparental forms of reproduction, as this hypothesis currently has the most support from natural populations. We also review the results from experimental evolution studies, which tend to show that exposure to novel environments can select for higher levels of sexual reproduction, but that sex decreases in frequency after populations become adapted to the previously novel conditions. In contrast, experimental coevolution studies suggest that host-parasite interactions can lead to the long-term persistence of sex. Taken together, the evidence from natural populations and from laboratory experiments point to antagonistic coevolution as a potent and possibly ubiquitous force of selection favoring cross-fertilization and recombination.

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

Cited by 28 publications

References 44 publications

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers

Gateway to genetic exchange? DNA double‐strand breaks in the bdelloid rotifer Adineta vaga submitted to desiccation

The ecology of sexual reproduction

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