Abstract
BackgroundAsexuality has major theoretical advantages over sexual reproduction, yet newly formed asexual lineages rarely endure. The success, or failure, of such lineages is affected by their mechanism of origin, because it determines their initial genetic makeup and variability. Most previously described mechanisms imply that asexual lineages are randomly frozen subsamples of a sexual population.Methodology/Principal FindingsWe found that transitions to obligate parthenogenesis (OP) in the rotifer Brachionus calyciflorus, a small freshwater invertebrate which normally reproduces by cyclical parthenogenesis, were controlled by a simple Mendelian inheritance. Pedigree analysis suggested that obligate parthenogens were homozygous for a recessive allele, which caused inability to respond to the chemical signals that normally induce sexual reproduction in this species. Alternative mechanisms, such as ploidy changes, could be ruled out on the basis of flow cytometric measurements and genetic marker analysis. Interestingly, obligate parthenogens were also dwarfs (approximately 50% smaller than cyclical parthenogens), indicating pleiotropy or linkage with genes that strongly affect body size. We found no adverse effects of OP on survival or fecundity.Conclusions/SignificanceThis mechanism of inheritance implies that genes causing OP may evolve within sexual populations and remain undetected in the heterozygous state long before they get frequent enough to actually cause a transition to asexual reproduction. In this process, genetic variation at other loci might become linked to OP genes, leading to non-random associations between asexuality and other phenotypic traits.
Highlights
The ubiquity of sexual reproduction is an evolutionary puzzle because asexuality should have major theoretical advantages [1,2]
Conclusions/Significance: This mechanism of inheritance implies that genes causing obligate parthenogenesis (OP) may evolve within sexual populations and remain undetected in the heterozygous state long before they get frequent enough to cause a transition to asexual reproduction
Other clones produced only cyclical parthenogenetic clones upon selffertilization. These percentages suggested that obligate parthenogens could be homozygous for a recessive allele, op causing a permanent loss of sexual reproduction: Heterozygotes, which still contain one wild-type allele (+/op clones), would be phenotypically cyclical parthenogens, but produce obligate parthenogenetic clones upon selfing at a 3:1 ratio (CP:OP), whereas homozygotes for the wild-type allele (+/+) are cyclical parthenogens, but should produce cyclical parthenogens only
Summary
The ubiquity of sexual reproduction is an evolutionary puzzle because asexuality should have major theoretical advantages [1,2]. The origin of new asexual lineages is typically viewed as a process that randomly freezes small proportions of the genetic variation of a sexual population [8,9]. This likely applies to the common modes of origin: hybridization, polyploidization, or infectious origin [7]. Gradual transitions towards asexuality would allow for hitchhiking effects, such that other traits may become linked to parthenogenesis Such gradual transitions to asexuality would be a plausible scenario if the propensity to reproduce (a)sexually was determined by additive genetic variation, or if asexuality was caused by a single non-dominant allele. Most previously described mechanisms imply that asexual lineages are randomly frozen subsamples of a sexual population
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