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Loss of Sexual Reproduction and Dwarfing in a Small Metazoan

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Loss of Sexual Reproduction and Dwarfing in a Small Metazoan

Claus-Peter Stelzer et al. PLoS One.

Abstract

Background: Asexuality 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 findings: We 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/significance: This 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.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Mendelian inheritance of obligate parthenogenesis in two strains of the rotifer Brachionus calyciflorus.
The figure shows an overview of all experimental clones, represented by numbered pie charts, which were propagated either by self-fertilization or experimental crosses. Roman numbers indicate successive sexual generations; Arabic numbers indicate individual clones of the two rotifer strains. Pie charts display the proportion of obligate vs. cyclical parthenogens among the sexually produced offspring clones of each clone. We analyzed 45 clones and determined the reproductive type in 88±5.2 (s.e.m.) of their sexual offspring clones, giving a grand total of 3962 analyzed clones.
Figure 2
Figure 2. Dwarfing in obligate parthenogenogenetic clones of the rotifer Brachionus calyciflorus.
Each symbol represents the mean value of egg size and female body size for different clone (Sample sizes for each clone: Eggs: n = 24±1.4; Females: n = 15±0.9; mean ± s.e.m.). Open symbols: obligate parthenogenetic clones (OP); closed symbols: cyclical parthenogenetic clones (CP), Circles: clones of the Florida strain; Triangles: clones of the Georgia strain. In total, 40 clones were analyzed (23 OP and 17 CP).

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