Research Article: Unisexual Reproduction Drives Evolution of Eukaryotic Microbial Pathogens

Date Published: October 31, 2013

Publisher: Public Library of Science

Author(s): Marianna Feretzaki, Joseph Heitman, Laura J. Knoll.


Partial Text

Genetic exchange occurs via horizontal gene transfer in bacteria and archea or sexual reproduction in fungal and parasitic eukaryotic microbes. Sexual reproduction is universal, or nearly so, in eukaryotes. Until recently, most eukaryotic microbial pathogens were thought to be clonal and asexual due to the absence of a compatible partner or the lack of morphological or population genetic evidence for sexual reproduction [1]. However, many of these eukaryotic pathogens have been found recently to have extant cryptic sexual cycles (Figure 1). Sex enables microbial pathogens to reshuffle their genomes, increase genetic diversity, purge deleterious mutations, and produce infectious propagules.

Sexual reproduction involving cells of opposite mating types or sexes comes with costs. Locating a compatible partner and undergoing mating and meiosis requires time and energy. In addition, sexual reproduction introduces genetic diversity, but in so doing rearranges well-adapted genomic configurations. In contrast, sexual reproduction involving cells of only one type (unisexual reproduction), via either mother-daughter cell-cell fusion or endoreplication, lowers the barrier to locating a compatible mating partner. Unisexual reproduction ameliorates the cost of losing a well-adapted phenotype in a particular niche while introducing more limited genetic diversity that may enhance the fitness of progeny in response to environmental changes, including drug treatments.

Among a broader group of microbial pathogens, the protozoan parasites also harbor extant sexual cycles that in some cases are now known to be cryptic or unisexual. Although these pathogens exhibit interesting and unusual sexual cycles, essentially nothing is as yet known about how sexes or mating types are established.

Unisexual reproduction has emerged as an adaptive mechanism in eukaryotic microbes, but also extends beyond unicellular organisms. In plants, self-pollination is surprisingly common. Transitions from cross-pollination to self-pollination are frequently observed; for example, the model plant Arabidopsis thaliana reproduces almost exclusively through self-pollination (∼99%) yet retains the ability to outcross at a low frequency (∼1%). Such transitions are thought to enable provincial species with restricted niches to emerge as successfully dispersed cosmopolitan species. In Bdelloid rotifers, males, an extant sexual cycle, and meiosis all appear to be absent, and these organisms are only known to reproduce via parthenogenesis [49]. More than 80 unisexual species of fishes, insects, reptiles, and amphibians also reproduce via parthenogenesis. Facultative parthenogenesis, where sexual species resort to reproduction in the absence of a compatible partner, is more widespread than obligate parthenogenesis. In vertebrates and mammals, even facultative parthenogenesis is very rare due to genomic imprinting. However, some isolated female sharks have given birth to live young (all daughters) in the absence of a male partner [50]. Facultative selfing has been documented not only in sharks but also in komodo dragons [51], and some species of domesticated birds. Moreover, genetic manipulation of the imprinting mechanisms in female mice resulted in healthy, live offspring produced via parthenogenesis under laboratory conditions [52]. Both unisexual reproduction and parthenogenesis can mitigate some of the costs associated with sex, but a common consequence is a reduced level of genetic exchange or diversity.

We now appreciate that eukaryotic microbial pathogens, including fungi and parasites, are not clonal and asexual, but rather have extant sexual cycles that are cryptic, parasexual, or even unisexual. Two of the three most common systemic human fungal pathogens (Candida and Cryptococcus) have retained extant sexual and parasexual cycles involving both bisexual and unisexual reproduction, which may provide a broader range of adaptive evolutionary strategies. Similar paradigms have now emerged for several eukaryotic parasites, suggesting this may be a general mode of adaptation for microbial pathogens, enabling them to preserve well-adapted genotypes. Given that sex is ubiquitous throughout the eukaryotic tree of life and yet we are confronted with a panoply of diverse mechanisms via which mating type (or sex) is specified and mating partners (or gametes) are distinguished and recognized, one possibility is that unisexual reproduction was the original ancestral form of sexual reproduction to which mating types and sexes were added later. If so, the finding that extant unisexual reproduction occurs in both fungal and parasitic pathogens may reflect a return to a more ancestral mode of reproduction rather than the emergence of an entirely new process promoting genetic change and exchange.




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