Spontaneous Speciation by Ploidy Elevation: Laboratory Synthesis of a New Clonal Vertebrate

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Spontaneous Speciation by Ploidy Elevation: Laboratory Synthesis of a New Clonal Vertebrate COMMENTARY Spontaneous speciation by ploidy elevation: Laboratory synthesis of a new clonal vertebrate Craig Moritz1 and Ke Bi Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720 he transition from diploid (2n) to polyploid (3n, 4n, and so forth), T a relatively common process in plants and some animal taxa, represents rapid speciation, as only rarely are hybrids able to form genetically bal- anced gametes (1). In vertebrates, poly- ploidy is often associated with asexual reproduction: sperm-dependent (gyno- genesis, hybridogenesis, and klepto- genesis) in amphibians and fish, and sperm-independent (parthenogenesis) in squamate reptiles (2). For the latter, ap- proximately 0.6% of known species are parthenogenetic, and, with few exceptions, these arose via hybridization between sexually reproducing progenitors (3). Given the relatively recent origin of most parthenogenetic taxa (2), it should then be possible to recreate parthenogenetic lineages of varying ploidy by hybridizing known progenitors in the laboratory, as has been achieved for some diploid hybrid plant species (4) and unisexual fish and frogs (see ref. 5). However, until now, this has not been achieved for parthenogenetic reptiles (e.g., ref. 6). In this context, the report by Lutes et al. (5) in PNAS is highly significant. Following from an earlier ob- servation of a potentially fertile, field- collected 4n female (7), Lutes et al. (5) Fig. 1. Phylogeny of Aspidoscelis for representative sexuals and unisexuals, based on figure 6 in ref. 9 crossed parthenogenetic 3n Aspidoscelis (A), and a possible route of ploidy elevation of unisexual salamanders in the Ambystoma laterale– exsanguis females and a sexual Aspidoscelis jeffersonianum complex (B) (19). Species in A are as follows: a, Aspidoscelis tesselata complex; b, Aspi- inornata male to produce three genera- doscelis neomexicana;c,Aspidoscelis laredoensis complex; d, intermediate ancestor; e, Aspidoscelis ne- tions of parthenogenetically reproducing otesselata complex; f, Aspidoscelis flagellicauda and Aspidoscelis sonorae complexes; g, Aspidoscelis 4n female lizards. Parthenogenetic re- exsanguis;h,Aspidoscelis opatae, Aspidoscelis uniparens, and Aspidoscelis velox complexes; i, 4n by A. production was confirmed by cytogenetic sonorae (female) × Aspidoscelis tigris (male; references 25, 26, and 28 in ref. 5); j, 4n by A. neotesselata × × analysis of female meiosis and multilocus (female) Aspidoscelis sexlineata (male; reference 27 in ref. 5); and k, 4n by A. exsanguis (female) A. inornata (male) (5, 7). *LJ is not a “true” hybrid directly derived by A. laterale × A. jeffersonianum (19); ╫ genotyping across multiple generations +sterile or unknown fertility; fertile (5) or potentially fertile (7). of the progeny. That a self-sustaining 4n lineage can be produced in the laboratory, but is not observed in nature, raises the with slightly heteromorphic sex chromo- commonly found in nature where 2n par- question of what constrains development somes, both male and female hybrids are thenogens and sexuals coexist, are typically of cascading polyploid series, as seen in observed, although these are sterile or of sterile (ref. 10; but see ref. 12). This has some invertebrates (8). Further, is it pos- unknown fertility (10). This is the case for been attributed to disruption of sex de- sible that 3n asexual lineages can form previously reported and cytogenetically termination, as these species have moder- a bridge in the evolution from 2n to 4n confirmed 4n hybrids between 3n parthe- ately to highly heteromorphic ZW sex sexually reproducing species (1)? nogens and 2n sexual males (10, 11). chromosomes (13). However, this does The whiptail lizards of the western Both these and the hybrids generated by not explain sterility of such hybrids in deserts of North America are remarkable Lutes et al. (5) have unbalanced (i.e., Heteronotia and Lepidodactylus geckos, in having a substantial diversity of both AABC) chromosome sets (Fig. 1A), so which lack heteromorphic sex chromo- 2n and 3n parthenogenetic lineages, all why the latter should be fertile but former somes (14, 15). In contrast, cascading of which arose via hybridization among not (or not known to be) is a mystery. sexual species (9) (Fig. 1A). Parthenoge- In other sexual–parthenogenetic com- netic lineages are often sympatric with plexes of reptiles, higher ploidy hybrids are Author contributions: C.M. and K.B. wrote the paper. congeneric sexual taxa, resulting in nu- also typically sterile. For example, Cauca- The authors declare no conflict of interest. merous reports of high ploidy hybrids in sian rock lizards of the genus Darevskia See companion article 10.1073/pnas.1102811108. nature (reviewed in refs. 10 and 11). As contain several diploid parthenogenetic 1To whom correspondence should be addressed. E-mail: Aspidoscelis have XY sex determination lineages of hybrid ancestry. Triploids, as [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1106455108 PNAS Early Edition | 1of2 Downloaded by guest on September 26, 2021 polyploidy elevation readily occurs in anced pairing between homologous (A–A of unisexual salamanders are character- some groups of amphibians [e.g., Bufo and B–B) rather than homeologous ized by complex ploidy and genome com- viridis group (16)] and fish (17, 18). For (A–B) chromosomes. As yet, all known binations, but all share a single origin, example, North American unisexual mole 4n hybrids of Aspidoscelis, including those and no recurrent hybridization between salamanders of the genus Ambystoma oc- generated by Lutes et al. (5), have un- known sexual sperm donors has generated casionally incorporate sperm from conge- matched chromosome sets (Fig. 1A). new unisexual lineages (19). Lutes et al. neric sexual males in syntopy to generate Therefore, and notwithstanding previous (5) find that the laboratory-produced 4n natural lineages with increasing ploidy efforts (6), it would be fascinating to hybrids are perfectly viable with no com- (19) (Fig. 1B). petitive disadvantage in prey capture when Why are there no such examples in Lutes et al. demonstrate housed with their progenitors. However, reptiles? One simple possibility is that as Lutes et al. (5) are aware, this does not successful elevation to higher ploidy is the potential to ensure that these newly formed 4n par- a rare event and is facilitated in unisexual thenogens are capable of persisting under fi amphibians and sh because of their con- generate higher-ploidy natural conditions, and in the face of tinuing dependence on sperm to initiate competitive pressure from both sexual the onset of development. In unisexual and unisexual progenitors in a constantly fi parthenogenetic sh, for example, this often leads to changing environment. variable amount of paternal leakage lineages of reptiles in The ability to produce self-sustaining, that ranges from microchromosomes to higher-ploidy hybrids between partheno- a whole genome set (17). However, in the laboratory. genetic and sexual lineages in the labora- some circumstances, hybrids between tory, but their absence in nature, raises parthenogenetic and sexual reptiles are many questions and also creates opportu- very common [e.g., as high as 50% (12)], extend these experiments to generate nities for further research. The relatively suggesting that this alone is not the whole 4n hybrids with balanced chromosome × recent ability to develop genomic resour- story. Another possibility is that such sets (e.g., A. sonorae A. inornata,or ces for such systems and, therefore, to transitions depend on intense selection for A. uniparens × Aspidoscelis burti, Fig. 1A). examine patterns of gene expression and rare balanced gametes and, thus, are more The results from Lutes et al. (5) dem- probable in taxa with high female fecun- onstrate the potential to generate higher- intergenomic interactions in sterile versus dity (1). ploidy parthenogenetic lineages of re- fertile hybrids relative to their partheno- A related question is whether unisexual ptiles in the laboratory. So, given that genetic and sexual progenitors offers triploidy is a bridge to formation of sexu- these particular taxa, A. exsanguis and A. a new window into often proposed, but ally reproducing tetraploids (1). Such inornata, are known to occur in sympatry still poorly understood, genetic constraints transitions have been observed in fish (10), why do we not see a self-sustaining on the evolution of parthenogenesis and (18), but how most sexual polyploid ver- 4n lineage in nature? One possibility polyploidy (20). tebrates (e.g., amphibians and fish) arose might be that very specific genomic com- binations of particular parental individuals ACKNOWLEDGMENTS. C.M. is supported by is poorly understood. In general, 4n sexual grants from the National Science Foundation. K.B. reproduction is most likely with matched are needed to initiate or to maintain uni- is supported by a Natural Sciences and Engineer- chromosome sets (AABB), allowing bal- sexuality (2). For example, populations ing Research Council postdoctoral fellowship. 1. Mable BK (2004) ‘Why polyploidy is rarer in animals 7. Neaves WB (1971) Tetraploidy in a hybrid lizard of the 14. Moritz C (1984) The origin and evolution of partheno- than in plants’: Myths and mechanisms. Biol J Linn genus Cnemidophorus (Teiidae). Brev Mus Comp Zool genesis in Heteronotia binoei (Gekkonidae). 1. Chro- – Soc Lond 82:453–466. 381:1–25. mosome banding studies. Chromosoma 89:151 162. 2. Avise JC (2008) Clonality: The Genetics, Ecology, and
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