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Genomic clues to an ancient asexual scandal.
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA.
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA.ORCID iD: 0000-0001-6112-9586
2007 (English)In: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 8, no 12, 232Article in journal (Refereed) Published
Abstract [en]

Despite abandoning meiosis, the bdelloid rotifers have persisted for millions of years and given rise to hundreds of species. Several mechanisms - allelic variants with different functions, high effective population size, and resistance to radiation - may contribute to their success.

Bdelloid rotifers are diploid aquatic microinvertebrates that live in fresh or brackish water, especially in ephemeral habitats prone to periodic desiccation. They are the only well documented lineage that has eliminated meiosis yet has persisted for many millions of years (more than 35 million years [1]) and undergone an adaptive radiation - nearly 400 species in three families. Maynard Smith [2] referred to them as an "evolutionary scandal" because they are the exception to the usual pattern that asexual lineages die out before undergoing extensive speciation.

The fact that asexuals are composed entirely of offspring-producing females gives them an intrinsic demographic advantage over sexual competitors whenever males do not help to produce offspring (referred to as the 'two-fold cost of sex' or the 'cost of producing males'). Evolutionary theory predicts, however, that obligate asexuals have a long-term evolutionary disadvantage, compared with sexuals, owing to a more pronounced 'Hill-Robertson effect', a reduction in the efficacy of natural selection that occurs because finite populations accumulate associations of linked genes (haplotypes) that interfere with selection [3, 4] (Figure 1).

Figure 1

The effect of genetic linkage on the effectiveness of selection. Consider two closely linked single nucleotide polymorphisms (SNPs A and B) with one of the 'alleles' at each site favored by selection (denoted by a superscript +). Selection acts more weakly on the 'interfering' haplotypes (A+B- and A-B+), where positive selection on one SNP is counterbalanced by negative selection on the other, compared with the 'reinforcing' haplotypes (A+B+ and A-B-), where selection on the two SNPs is complementary. This disparity causes interfering haplotypes to persist longer after they have accumulated by chance in finite populations. See Box 1 for further details.

The Hill-Robertson effect arises when selection acts simultaneously at multiple linked sites (Figure 1). In this case, the fate of a mutation depends not only on its own selective value but also on that of its genetic backgrounds. Selection on genetic backgrounds introduces 'noise', which makes selection on a mutation less efficient. A similar interaction occurs between selection and random genetic drift, with smaller population sizes increasing the noise generated by drift. The cost of the Hill-Robertson effect in asexuals can be expressed as a reduced effective population size (N e , the size of an idealized, random-mating population with only chance fluctuations in family sizes) compared with the actual population size (census size, N; see Box 1 for further details). Because the strength of the Hill-Robertson effect increases with tighter linkage, non-meiotic species like bdelloid rotifers, in which 'interfering' haplotypes cannot be routinely broken up, should have a much reduced N e compared with their sexual competitors with similar census sizes, and should hence experience less effective selection. All else being equal, the bdelloids' ability to compete with sexuals should erode over time, leading to their eventual extinction. This has not happened, so the bdelloids must have one or more compensating advantages. Several recent studies indicate how bdelloids may have achieved their "scandalous" status.

Place, publisher, year, edition, pages
2007. Vol. 8, no 12, 232
National Category
Biological Sciences Evolutionary Biology Zoology
Identifiers
URN: urn:nbn:se:liu:diva-137232DOI: 10.1186/gb-2007-8-12-232PubMedID: 18177507OAI: oai:DiVA.org:liu-137232DiVA: diva2:1094282
Available from: 2017-05-09 Created: 2017-05-09 Last updated: 2017-05-18Bibliographically approved

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