Archives for July 2019

Approximately 90 vertebrate species are known to exist as unisexual populations, that is, consisting of reproducing females (Lampert & Schartl, 2010). All of these are restricted to fish, amphibian and reptile species (Figure 1). An all-female reproducing population has advantages since every individual can carry young so the population has the potential to grow at a faster rate than bisexual populations, where the male only donates sperm and does not produce offspring. Since this has a distinct advantage it is perhaps unusual that unisexual populations are so rare. However, the main cost of being unisexual is the loss of genetic recombination which occurs in male and female bisexual populations. This is crucial in providing genetic stability, preventing accumulation of mutations and providing opportunities for adapting to a changing environment. Therefore, unisexual species do not occur widely amongst vertebrates.

Unisexual reproduction is often referred to as parthenogenesis, which is “reproduction in the absence of fertilization of the egg” (Lampert & Schartl, 2010). However, there are different forms of parthenogenesis which do allow some genetic exchange. True parthenogenesis occurs in females in the complete absence of males. This is incredibly rare and is known only from a handful of vertebrate species. However, one other type of parthenogenesis, known as gynogenesis, occurs when male sperm is used to trigger development of the female’s embryo. In this circumstance, the female does not incorporate any of the sperm’s genetic material and she uses all of her own so the sperm’s genome is redundant. However, in some situations, known as kleptogenesis, the female may incorporate some of all of the sperm’s genome thus resulting in offspring that have, 2, 3 or 4 times the amount of genetic material (diploid, triploid or tetraploid respectively) (Bogart et al., 2007). Since they ‘steal’ gametes of sexual species for their own reproduction, they are considered to be sexual parasites of their (usually parental) host species (Mikulíček et al., 2014). A third type of parthenogenesis is hybridogenesis where the eggs of a unisexual female are fertilised by the sperm of a closely related bisexual male. However, this genetic material is only incorporated into the new genome for one generation and is excluded when this female produces her own eggs (Lambert et al., 2010).  Therefore, only maternal genes are passed onto subsequent generations. All these forms of parthenogenesis result in the inclusion of ‘fresh’ genetic material into the female thus improving the fitness of populations and increasing their robustness to resist diseases.

Two main groups of amphibians are known to exhibit unisexuality. Unisexual mole salamanders (genus Ambystoma), occur in North America and generally have between two and five times the normal complement of genetic material compared to bisexual Ambystomid salamanders (Figure 2). These Ambystomid unisexual individuals are the oldest known group of unisexual vertebrates, having occurred for over 5 million years (Gibbs & Denton, 2016). The DNA in the nucleus of unisexual individuals is usually composed of genetic material from several species including: the blue spotted salamander (Ambystoma laterale), Jefferson salamander (A. jeffersonianum), small-mouthed salamander (A. texanum) and tiger salamander (A. tigrinum). This leads to a large range of possible genetic combinations with genetic material from the blue spotted salamander being present in most unisexual individuals. Female unisexual salamanders require sperm from a bisexual salamander species which are living in the same area to initiate reproduction. However, they can then either use the sperm solely to activate egg development (i.e. gynogenesis) or incorporate the sperm genome into the resulting offspring (Bogart et al., 2007). If genetic material from the sperm is used during reproduction, either the DNA is retained, resulting in the offspring with additional genetic material, or it is replaced. In a recent study, Gibbs & Denton (2016) studied the genetic exchange in unisexual populations of Ambystomid salamanders to try and explain how unisexual populations have persisted in the environment for 5 million years. They found that unisexual individuals gain enough genetic material through the occasional process of obtaining DNA from males to allow populations to remain robust and able to withstand environmental change. Therefore these individuals gain all the advantages of being unisexual, with also some of the advantages of sexual reproduction i.e. genetic mixing.

One of the well-known breeding systems involving hybridogenesis is that of the water frog (Pelophylax esculentus) complex (Ranidae), widely distributed in Europe, which has considerable variation in types of hybridogenesis (Figure 3). The Pelophylax esculentus complex consists of two parental species, the marsh frog (P. ridibundus) and pool frog (P. lessonae), and their hybridogenetic hybrid the edible frog (P. esculentus). Edible frogs usually contain genetic material from both parental species. In most of its range, the edible frog reproduces hybridogenetically with the pool frog. However, during reproduction the pool frog genome is lost in the eggs and sperm. Therefore, pool frog DNA is not passed down to subsequent generations and the edible frog is considered a sexual parasite (Christiansen et al., 2005). However, many variations of this mating system occur across the species’ range. In most cases, female edible frogs will use the genetic material from the male, but it is not fully incorporating it into its genome. Due to the unusual genetic combining during hybridogenesis the presence of edible frogs can result in loss of the parental pool frog and marsh frog genotypes and is a potential conservation problem when it occurs in these populations.

Overall, unisexuality in amphibians represents a unique form of reproduction that has remained evolutionarily stable for several million years through occasional genetic mixing from the same or closely related species. Ambystomid salamanders and water frogs have proved highly successful at unisexual reproduction which is otherwise a rarely used breeding strategy amongst vertebrates.

References

Bogart, J.P., Bi, K., Fu, J., Noble, D.W.W. & Niedzwieckim, J. (2007) Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes. Genome, 50: 119–136.

Christiansen, D.G., Fog, K., Pedersen, Bo V. & Boomsma, J.J. (2005) Reproduction and hybrid load in all-hybrid populations of Rana esculenta water frogs in Denmark. Evolution, 59 (6): 1348–1361.

Gibbs, H.L., & Denton, R.D. (2016) Cryptic sex? Estimates of genome exchange in unisexual mole salamanders (Ambystoma sp.). Molecular Ecology, 25: 2805–2815.

Lampert, K.P. & Schartl, M. (2010) A little bit is better than nothing: the incomplete parthenogenesis of salamanders, frogs and fish. BMC Biology, 8: 78-80.

Mikulíček, P., Kautman, M., Kautman, J. & Pruvost, N.B.M. (2014) Mode of hybridogenesis and habitat preferences influence population composition of water frogs (Pelophylax esculentus complex, Anura: Ranidae) in a region of sympatric occurrence (western Slovakia). Journal of Zoological Systematics & Evolution Research. doi: 10.1111/jzs.12083.