Schmidt, B. R. 1996. Sexual and asexual reproduction in vertebrates. Trends in Ecology and Evolution 11: 253-254.


Full text (without references): The maintenance of sexual reproduction, discussed by Hurst and Peck in their recent TREE article, is a central problem in evolutionary biology. Although asexuality has advantages in the short term, it is relatively rare. Thus, it is important to understand why sex predominates. Constraints against unsexuality are a possible cause. Here, I discuss constraints in vertebrates that prevent unisexual reproduction and force them to maintain sexual reproduction. These constraints may be a consequence of intragenomic conflicts. This idea deserves more attention than Hurst and Peck have drawn to it.
There is no naturally occurring unisexual vertebrate species. All parthenogenetic, gynogenetic or hybridogenetic vertebrates are of hybrid origin. This suggests that there are strong genetic or cytological mechanisms in vertebrates that prevent unisexual reproduction, and that hybridization is needed to overcome them. The mechanism that is eliminated by hybridzation is likely to be the mechanism that prevents unisexual reproduction. Under the pressure of mutations for parthenogenesis, males may have evolved mechanisms that prevent offspring development from parthenogenetic females, for example, paternal inheritance of centrioles in frogs. Intragenomic conflicts may also have lead to the evolution of sexes und uniparental inheritance of organelles and to genomic imprinting that prevents unisexuality in mammals. Although parthenogenesis may not be possible anymore, meiotic drivers may still attempt to transmit a genome clonally. Such meiotic drivers may reappear in the hybrid owing to the lack of suppression. If they are meiotic drivers of X chromosomes against Y chromosomes that are suppressed in the parental species, then they may reappear in the hybrid, and lead to unisexuality or clonal transmission of a genome.
Hybridogenetic frogs illustrate this hypothesis. In one parental species (Rana ridibunda) of hybridogenetic frogs, there seems to be meiotic drive of the X chromosomes against the Y chromosome (and possibly the other chromosomes inherited from the sire), which appears to be suppressed. This meiotic drive may be an attempt to annihilate the genome of the other parent, or a form of sex ratio distortion. In the hybridogenetic hybrid, the R. ridibunda genome (always associated with the X chromosome) drives against the genome of the other parental species, excludes it from the germline premeiotically, and transmits itself clonally to all offspring. Frogs cannot reproduce parthenogenetically, but this mechanism allows hybridogenetic hybrids to transmit their genomes clonally. Thus, whereas the parental species reproduce sexually, the hybrid reproduces unisexually due to the result of meiotic drive, but still depends on a sexual hang-up.
Although all vertebrates require hybridization for unisexuality, this requirement appears not to be an ancestral state of the vertebrate clade. The form of unisexuality after hybridization varies among vertebrate groups. The fact that there is geographic variation in the ability of R. ridibunda to produce hybridogenetic hybrids, and that some (but not all) unisexual Heteronotia geckos, unisexual Cnemidophorus lizards, and unisexual Ambystoma salamanders, seem to have originated from a few females and are geographically restricted suggests that many attempts at meiotic drive may be relatively recent. Thus, intragenomic conflicts may be widespread, may still be going on and they may be an important reason for the maintenance of bisexuality in vertebrates (and probably more organisms).


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Peter Beerli (beerli@scs.fsu.edu)