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Keywords:

  • asexual;
  • gynogenesis;
  • hybridogenesis;
  • parthenogenesis;
  • Poecilia;
  • sexual reproduction

Abstract

  1. Top of page
  2. Abstract
  3. Acknowledgements
  4. References

All-female ‘species’ of fish have been shown to be great models in ecological and evolutionary studies because of the insights they can provide into the origin and evolution of asexuality, the ecology of hybrids, associations between genotype and environment, and the maintenance of sex. Gynogenetic organisms that evolved from sexual ancestors, and combine the disadvantageous traits from sexuality and asexuality, have long baffled evolutionary biologists trying to understand their origin and persistence with their sympatric sexual counterparts. In this issue, a new study using an integrated molecular phylogenetic and classical genetic approach has uncovered compelling evidence regarding the obscure asexual origin of the Amazon molly, Poecilia formosa. By performing an extensive phylogeographic analysis, Stöck et al. (2010) provide evidence that the Amazon molly arose only once within its history, with monophyly being strongly supported by mitochondrial DNA and microsatellite analyses. This result, combined with an elaborate failed attempt to resynthesize the lineage, suggests that vertebrate gynogens such as the Amazon molly are not rare because they are at a disadvantage to their sexual counterparts, but because the genomic conditions under which they arise are rare. Organisms that apparently combine the disadvantages of both sexuality and asexuality remain difficult to understand from both an ecological and an evolutionary perspective, and Stöck et al. (2010) highlight several outstanding important questions. Nonetheless, given that we now have a better knowledge of the origin and history of this unique ‘species’, this should allow researchers to better understand how these frozen F1’s can persist amidst the masterpiece of nature.

Following the first contributions of Williams (1975) and Maynard Smith (1978) on the paradox of sex, the evolution of sexuality has often been considered to be ‘a masterpiece of nature’ (Bell 1982) and an ‘enigma’ (Otto 2009). Yet, the evolution and maintenance of sex remain unresolved (Otto 2009), largely because of the difficulty reconciling such a costly evolutionary strategy. For instance, the evolution of recombination would have had to initially deal with invading asexuals (Doncaster et al. 2000). Sex is also expensive when considering the ecological (e.g., sexually transmitted diseases, mate choice, energy allocation) and mechanical (e.g., switching from mitotic to meiotic division) costs of finding a mate. The true cost of sex is often considered to be the continual reduction in half of the number of genes passed on to the next generation (Williams 1975). Additionally, two individuals are required to restore the parental state, so females must produce males (Maynard Smith 1978). Finally, the act of recombination itself actually breaks apart favourable gene combinations that may have been maintained by selection (Bell 1982). So why does nature have so much sex when the costs are so high? When considering that asexual reproduction has been documented in only ∼0.1% of animal species (Vrijenhoek 1998) while <1% of the 300 000 angiosperms are considered asexual (Whitton et al. 2008), sex is indeed an enigma (Otto 2009). Recent evidence suggests this paradox can be reconciled when we consider the advantages of sex in a dynamic world with finite resources, leading to certain conditions that allow for its evolution, namely that sex may provide the ultimate mechanism to re-introduce variation (Otto 2009). However, relatively less attention has been paid to the persistence of recently evolved asexuals, the other side of the sex paradox.

With few exceptions, virtually all extant animal and plant asexuals are found at the tips of the tree of life, leaving biologists left to contend with these baffling organisms that in most cases evolved from sexual ancestors but arguably cannot even be considered species (Mayr 1963). In sharp contrast to sexual reproduction, asexuality leads to the replication of identical progeny from a single ancestor. Parthenogenesis, or ‘virgin reproduction’, stems from only maternal contributions (Schlupp 2005). Gynogenesis occurs when the sperm triggers parthenogenesis (Fig. 1). Hybridogenesis is a variant of the sperm-dependent process when haploid cells that are produced fuse with sperm, or in some cases, the male chromosomes are literally tossed from the egg leading to only the maternal genome being transmitted to the next generation (gametogenesis) (Fig. 1). Interestingly, most gynogenetic vertebrates are of hybrid origin (Vrijenhoek 1998). Consequently, such species start out with extremely high heterozygosity and are sometimes referred to as ‘frozen F1’s’ (Vrijenhoek 1979). Gynogens are interesting models because they evolve from their sexual ancestors and combine the disadvantageous traits from sexuality and asexuality. At a genetic level, gynogens deal with genetic decay, while at an ecological level, they still have to deal with the considerable risks of finding (or stealing) a mate (a partner that does not really stand to benefit either). Nonetheless, some have hypothesized that newly evolved asexual gynogens may have some advantages over their ancestral sexual counterparts when colonizing new habitats (Vrijenhoek 1998; Avise 2008). In addition to the fast propagation of asexuals, the peculiar mode of gynogenetic reproduction sometimes allows for introgression of genetic material via ‘paternal leakage’ from sexually reproducing mating partners (Stöck et al. 2010). Moreover, Vrijenhoek (1979) proposed a ‘frozen niche variation’ model based on the evolution of niche breadth, whereby clone colonizers may be better suited for ecological release because, unlike their sexual counterparts, they are not required to shuffle their genotypes every generation. These frozen F1’s may also express ‘spontaneous heterosis’ (Wetherington et al. 1987). Miller et al. (2006) assume that these asexuals can arise multiple times. These are interesting arguments that contribute to the ongoing interest of studying gynogen evolution, especially in the context of trying to understand the scarcity and persistence of asexuals (Vrijenhoek 1994).

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Figure 1.  Schematic of female modes of the reproduction in fish. In regular sexual reproduction, sperm from males fertilizes haploid gametes from females. Gynogenesis is a variant of the process that occurs when the sperm triggers parthenogenesis, whereas hybridogenesis is a hemiclonal form of inheritance, whereby even though the sperm truly fertilizes the egg, only the maternal chromosome is transmitted. M refers to maternal contributions, whereas P refers to paternal contributions (see also Schlupp 2005).

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There are several well-known examples of gynogenesis in vertebrates and invertebrates (Beukeboom & Vrijenhoek 1998; Schlupp 2005), but the best known is the molly, a euryhaline brackish water fish from the genus Poecilia more commonly recognized as a popular tropical aquarium fish (Vrijenhoek 1998) (Fig. 2). One species, Poecilia formosa, is not as popular in tropical aquaria but has long been recognized morphologically as having a hybrid origin (Hubbs & Hubbs 1932) and reproducing gynogenetically via sperm from a closely related species (Vrijenhoek 1994). Molecular analyses confirmed the hybrid state and found that the maternal ancestor is the Atlantic molly, P. mexicana, while the paternal ancestor appears to be the sailfin molly, P. latipinna (Avise et al. 1991). The most recent molecular estimates suggest a clonal existence for almost 300 kya or over 800 000 generations. However, whether a single, multiple or ongoing hybridization events led to the formation of the Amazon molly has remained a mystery as both parental species are sympatric in the Atlantic coastal drainages of northern Mexico (Schlupp et al. 2002).

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Figure 2.  (a) Poecilia formosa female (upper) ‘stealing’ sperm from a courting P. mexicana male (lower). Photograph: Manfred Schartl (b) Poecilia formosa from the Rio Purificación. Photograph: Manfred Schartl.

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Now, in a unique approach that combines extensive molecular phylogenetic and classical genetic approaches to address these questions, a study by Stöck et al. (2010) in this issue has uncovered new evidence regarding the obscure asexual origin of the Amazon molly. Stöck et al. performed a standard phylogenetic analysis over the entire natural range of all Poecilia species, including individuals from P. latipinna, P. mexicana, P. limantouri and P. formosa. Their data confirmed the close relationship between P. mexicana and P. formosa (Avise et al. 1991). Moreover, the authors discovered that a single mutational step in a bisexual P. mexicana haplotype from the east coast of Mexico likely became the geographically most widespread haplotype of the hybridized all-female P. formosa. The microsatellite data were highly supportive of a monophyletic origin and refuted any multiple recent or ongoing hybridizations generating new P. formosa lineages.

Jerry Coyne once quipped at the 2006 American Genetics Association Speciation Genetics conference, ‘It ain’t genetics unless you do a cross’. Accordingly, Stöck et al. (2010) followed up the phylogenetics with a classical genetics approach in an attempt to resynthesize P. formosa by mating fish from putative parental species. In over 600 F1 offspring, only 17% were males. The authors used over 200 of these F1 females in testcrosses with Black molly males, generating over 3100 offspring. Every individual exhibited a characteristic black spotting phenotype (Fig. 3), the telltale expression of a dominant paternal pigmentation gene indicating sexual reproduction. Their failure to resynthesize P. formosa is consistent with several earlier unsuccessful attempts (Turner et al. 1980). However, all but two F1 hybrids between P. formosa’s ancestors exhibited a prerequisite for the evolution of gynogenesis (Lampert et al. 2007), namely the production of diploid eggs, albeit with low reproductive rates as most testcross offspring were triploid.

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Figure 3.  Hypothetical scenario for the origin of P. formosa. (a) Most successful mating attempts between P. mexicana females and P. latipinna males result in (b) hybrids of both sexes. Apparently, one such cross 300 kya (c) produced the female-only gynogenetic P. formosa.

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It is reasonable to assume that gynogenesis is tricky business genetically, but these data actually shed new light on the evolution of gynogenesis. Namely, a monophyletic origin together with an inability to resynthesize P. formosa supports the hypothesis that asexual vertebrates are perhaps not rare because they are at a disadvantage to their sexual counterparts, but simply because the conditions under which they can arise are rare. Evolving from sexual meiotic reproduction to ameiotic unisexuality is evidently very difficult and does not happen very often, at least not in natural populations of Poecilia species. Once it does occur, however, these frozen F1’s may apparently be every bit as successful as their ancestors, at least over the evolutionary time scales observed in P. formosa. The question now remains: if the origin of asexual gynogens is such a rare event, how long can the species coexist with its sexual ancestors?

It is difficult to reconcile organisms that apparently combine the disadvantages of both sexuality and asexuality and, of course, this study points to several important questions that remain. First, the high number of genotypes detected in the frozen asexual mollies, in this study and others, remains puzzling but may provide clues to the persistence of the lineage. For instance, Vrijenhoek (1978) proposed that asexual organisms might have sufficient clonal diversity in some instances to provide the variation necessary to occupy broad heterogenous adaptive zones. Second, given that their origin is such a rare event, many genomic changes are likely necessary to bring about the full process of gynogenesis (Vrijenhoek 1994; Schlupp 2005), especially if we consider that such changes need to be present in a single hybrid animal to become the ancestor of an asexual lineage. What those genetics changes are remains a mystery, but should now be possible to explore given recent advances in sequencing technologies. Third, sperm dependency is the defining feature of gynogens, yet the ecological consequences of this dependency remain poorly understood. Finally, and perhaps, most importantly in the context of their persistence, we still lack an understanding of the ecological consequences of sexual and asexual coexistence, especially given the hypothesized short-term ecological advantages of asexuality. This study suggests that it may be possible to address this question through direct comparisons of sexual and asexual species with known phylogenetic relationships in some vertebrates, especially Poecilia spp. Doing so could also offer insight into the maintenance of sex (Schlupp 2005).

Overall, in a very nice integration of phylogenetics and classical genetics using the Amazon molly system, Stöck et al. (2010) find evidence that the 0.1% of extant asexual vertebrate taxa might be rare not because they suffer the long-term consequences of clonal reproduction, but because they are only very rarely formed because of complex genetic preconditions necessary to produce viable and fertile clonal genomes. This ‘rare formation hypothesis’ provides an interesting explanation for the rarity of asexual species, which—once arisen—may be ecologically very successful and persistent (Vrijenhoek 1998). Yet, admittedly, if these asexual species tend to be found at the tips of the tree of life and do not speciate, this implies their evolutionary trajectories may be bleak. Thus, it would still be relevant to know more about the transition rates of asexuality from sexuality to better understand their origin and offer a more robust estimate of their longevity in evolutionary timescales. Nonetheless, Vrijenhoek (1994) argued that the stage was set for using these well-characterized animals in environmental studies and that only time would tell whether they are widely adopted. This new study by Stöck et al. (2010) will surely increase the attention on this remarkable ‘species’.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Acknowledgements
  4. References

The authors thank an anonymous reviewer for their comments that improved the manuscript. SMR and SMV are funded by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada (NSERC).

References

  1. Top of page
  2. Abstract
  3. Acknowledgements
  4. References