- Open Access
A little bit is better than nothing: the incomplete parthenogenesis of salamanders, frogs and fish
© Lampert and Schartl; licensee BioMed Central Ltd. 2010
- Received: 18 May 2010
- Accepted: 9 June 2010
- Published: 3 August 2010
A re-examination of the mitochondrial genomes of unisexual salamander lineages, published in BMC Evolutionary Biology, shows them to be the oldest unisexual vertebrates known, having been around for 5 million years. This presents a challenge to the prediction that lack of genetic recombination is a fast track to extinction.
See research article http://www.biomedcentral.com/1471-2148/10/238
- Mitochondrial Genome
- Maternal Genome
- Bisexual Species
- Mole Salamander
- Unisexual Vertebrate
The question then arises: are the hypotheses about the consequences of the absence of recombination wrong, or are the age estimates? Most probably, both are correct. The solution to this paradox comes from the fact that many unisexual vertebrates have specialized ways to circumvent the lack of meiotic recombination in their nuclear genome (see ).
Although all unisexual female reproduction is often loosely called parthenogenesis (reproduction in the absence of fertilization of the egg), true parthenogenesis is much more restricted. Defined as the production of offspring by virgin females in the total absence of males, true parthenogenesis results in genetically identical clonal populations. In this exclusivity, true parthenoforms of vertebrates are only found in unisexual lizards and the single unisexual snake species known to date. The unisexual fish and amphibians, in contrast, reproduce by variations of parthenogenesis, which are incomplete and genetically leaky compared with true parthenogenesis.
A third form of leaky parthenogenesis found in some vertebrates is hybridogenesis. In this mode of reproduction, haploid oocytes are produced without meiosis. The oocytes are fertilized by sperm from a closely related bisexual species but the male genetic material is only present for a single generation; it is excluded during oocyte production and consequently is not passed on to the next generation, and so the oocytes always exclusively contain a maternal genome.
These leaky forms of parthenogenesis very rarely, or not so rarely, allow the inclusion of paternal genetic material in the oocyte. The consequence is a constitutive or occasional addition of 'fresh' genetic material that can slow down the degeneration process of Muller's ratchet and increase genetic diversity.
This then raises the question: why are unisexual vertebrate species so rare if they have found ways to decrease the negative impact of having no meiosis but simultaneously enjoy the advantage of enhanced population growth? An attractive hypothesis is that unisexuals are so rare not because they are under considerable disadvantage compared to their bisexual competitors, but because the genomic conditions under which they can arise are extremely rare . Evidence for this comes from a study on the gynogenetic Amazon Molly, P. formosana . The diploid genome of the asexual biotype is composed of one copy from its maternal ancestor, P. mexicana, and one copy from its paternal ancestor, P. latipinna. Both these species still live together at some places in northeast Mexico, and there has been ample opportunity for hybridization. In the laboratory, hybrids between these two species, carrying both genomes, are easily produced, but they are not the expected gynogens of the P. formosa type. P. formosa, like the mole salamanders, has been found to be monophyletic and of rather ancient origin. All this shows that the hybrid composition of the genome is not on its own sufficient to initiate asexuality. Only certain combinations of individual genomes from the genome pools of both species, and possibly additional mutations in the hybrid, can bring about the switch from bisexual to unisexual reproduction.
The paper by Bi and Bogart  is a crucial cornerstone to our understanding of the biology of unisexual vertebrates and the evolution of asexuality versus sexuality in general. The reproductive mode of kleptogenesis in the mole salamanders and the other mechanisms of incomplete parthenogenesis in unisexual fish and other amphibians have obviously ensured their long-term survival, and tell us that 'a little bit of sex' gives these organisms the best of both worlds - just enough genetic variation in addition to the mutations that generate new genotypes also in asexuals, plus the superior mode of propagation in the absence of males.
We thank the Deutsche Forschungsgemeinschaft for support.
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