Genomic signatures of ancient asexual lineages

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267

Sexual reproduction and clonality in eukaryotes are mostly seen as exclusive, the latter being rather exceptional. This view might be biased by focusing almost exclusively on metazoans. We analyze and discuss reproduction in the context of extant eukaryotic diversity, paying special attention to protists. We present results of phylogenetically extended searches for homologs of two proteins functioning in cell and nuclear fusion, respectively (HAP2 and GEX1), providing indirect evidence for these processes in several eukaryotic lineages where sex has not been observed yet. We argue that (i) the debate on the relative significance of sex and clonality in eukaryotes is confounded by not appropriately distinguishing multicellular and unicellular organisms; (ii) eukaryotic sex is extremely widespread and already present in the last eukaryotic common ancestor; and (iii) the general mode of existence of eukaryotes is best described by clonally propagating cell lines with episodic sex triggered by external or internal clues. However, important questions concern the relative longevity of true clonal species (i.e., species not able to return to sexual procreation anymore). Long-lived clonal species seem strikingly rare. We analyze their properties in the light of meiotic sex development from existing prokaryotic repair mechanisms. Based on these considerations, we speculate that eukaryotic sex likely developed as a cellular survival strategy, possibly in the context of internal reactive oxygen species stress generated by a (proto) mitochondrion. Thus, in the context of the symbiogenic model of eukaryotic origin, sex might directly result from the very evolutionary mode by which eukaryotic cells arose.reactive oxygen species | evolution | protists | eukaryotes | sex

Section: Sex In Eukaryotic Microorganisms: More Voyeurs Neededmentioning

confidence: 98%

Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life

Speijer

Lukeš

Eliáš

2015

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267

“…In particular, the absence of recombination and genetic exchange in apomictic obligate asexual diploids produces a genealogical history that essentially contains two parallel lineages, one for each formerly allelic copy of the genome. The formerly allelic gene copies within an obligate asexual individual therefore become increasingly divergent over time (19)(20)(21). This characteristic molecular signal of obligate asexual reproduction has been used as evidence for the ancient obligate asexuality of bdelloid rotifers (20).…”

mentioning

confidence: 99%

Molecular signatures for sex in the Placozoa

Signorovitch

Dellaporta

Buss

2005

Placozoans, the simplest free-living animals, have never been observed to reproduce sexually. Here, we describe molecular evidence for sexual reproduction within one clade of the Placozoa. In a population sample of 10 individuals, within-individual and overall nucleotide diversity were similar to each other and consistent with levels observed in sexually reproducing species. Intergenic recombination as well as the sharing of alleles between heterozygous and homozygous individuals was also observed. These hallmarks of sexual reproduction establish that sex is indeed present in this phylum.obligate asexual ͉ sexual reproduction ͉ Trichoplax ͉ basal metazoan ͉ Belize

“…Ancient taxa in which sexual reproduction is unknown have therefore attracted attention as systems whose study may shed light on what has allowed them to avoid extinction and successfully evolve. Of these, the group for which evidence of ancient asexuality is strongest is the class Bdelloidea of the phylum Rotifera (4).…”

mentioning

confidence: 99%

Evidence for degenerate tetraploidy in bdelloid rotifers

Welch

Meselson

2008

118

Rotifers of class Bdelloidea have evolved for millions of years apparently without sexual reproduction. We have sequenced 45-to 70-kb regions surrounding the four copies of the hsp82 gene of the bdelloid rotifer Philodina roseola, each of which is on a separate chromosome. The four regions comprise two colinear gene-rich pairs with gene content, order, and orientation conserved within each pair. Only a minority of genes are common to both pairs, also in the same orientation and order, but separated by gene-rich segments present in only one or the other pair. The pattern is consistent with degenerate tetraploidy with numerous segmental deletions, some in one pair of colinear chromosomes and some in the other. Divergence in 1,000-bp windows varies along an alignment of a colinear pair, from zero to as much as 20% in a pattern consistent with gene conversion associated with recombinational repair of DNA double-strand breaks. Although pairs of colinear chromosomes are a characteristic of sexually reproducing diploids and polyploids, a quite different explanation for their presence in bdelloids is suggested by the recent finding that bdelloid rotifers can recover and resume reproduction after suffering hundreds of radiation-induced DNA double-strand breaks per oocyte nucleus. Because bdelloid primary oocytes are in G 1 and therefore lack sister chromatids, we propose that bdelloid colinear chromosome pairs are maintained as templates for the repair of DNA double-strand breaks caused by the frequent desiccation and rehydration characteristic of bdelloid habitats.asexual reproduction ͉ genome structure ͉ evolution of sex ͉ gene conversion ͉ anhydrobiosis T here are numerous hypotheses and theoretical models but no general agreement about what selective factors and underlying mechanisms are responsible for the nearly universal occurrence of sexual reproduction among animals and plants and the relatively early extinction of lineages that abandon it (1-3). Ancient taxa in which sexual reproduction is unknown have therefore attracted attention as systems whose study may shed light on what has allowed them to avoid extinction and successfully evolve. Of these, the group for which evidence of ancient asexuality is strongest is the class Bdelloidea of the phylum Rotifera (4).Bdelloid rotifers are common invertebrates a few tenths of a millimeter long characteristically found in the water films of mosses and lichens, in temporary freshwater pools, and in other ephemerally aquatic habitats. They are able to thrive in such settings because they can survive desiccation at any stage of their life cycle by entering a metabolically quiescent state of anhydrobiosis (5). Distinguished by their ciliated head structure, bilateral ovaries, and jaw-like mastax, they have ganglia; muscles; digestive and secretory systems; photosensitive and tactile sensory organs; and structures for feeding, crawling, and swimming (6, 7). The class includes 461 described species classified in four families and 19 genera (8). The identification to the famil...