An ancient clonal lineage in the fish genus Poeciliopsis (Atheriniformes: Poeciliidae).

Abstract

Genetic diversity in mtDNA was assd within the unisexual (all female) hybridogenetic fish Poecdiopsis monacha-occidentalis and the two sexual species from which it arose. Results confirm that P. monacha was the maternal ancestor and that paternal leakage of P. occidentals mtDNA has not occurred. Of particular interest is the high level of de novo mutational divergence within one hybridogenetic lineage that on the basis of independent zoogeographic considerations, protein electrophoretic data, and tissue gaftng analysis is of monophyletic (single hybridization) origin. Using a conventional mtDNA clock calibration, we estimate that this unisexual clade might be >100,000 generations old. Contrary to conventional belief, this result shows that some unisexual vertebrate lineages can achieve a substantial evolutionary age.Clonally reproducing organisms are believed to have short evolutionary life-spans due to a presumed lack of sufficient genotypic diversity for adaptive change to variable environments (1-3) or to an accumulation of deleterious mutations and gene combinations that cannot be purged in the absence of recombination (2,4). However, many unisexual (all female) vertebrate populations are not devoid of genetic variation, and some clearly enjoy short-term ecological success relative to their sexual progenitors (5). Can such unisexual lineages also persist over long evolutionary time scales?Genetic studies reveal that virtually all unisexual vertebrates arose recently from hybridization involving congeneric sexual species (for reviews, see ref. 6). Clonal diversity within a unisexual "biotype" (a particular combination of two or more heterospecific genomes) results primarily from multiple, independent, hybrid origins; however, additional variation can accrue within independent lineages after their inception via polyploidization and mutation (5).Inferences concerning the evolutionary age of unisexual organisms must avoid confounding postformational processes that are indicative of an old lineage with genetic diversity arising from multiple hybrid origins. However, incomplete sampling of the sexual ancestors and incomplete assessment of diversity in the unisexual populations often defeat attempts to discriminate multiple origins from postformation processes. For example, unisexual lineages often are marked by unique alleles not observed in samples of their sexual relatives (7-11). Although unique alleles might represent postformational mutations, most authors interpret them as "orphan alleles," variants that exist in unsampled sexual populations or that might have existed in extinct sexual progenitors (12). With this conservative approach, postformational mutations could be overlooked and potential evidence for antiquity could be discounted.The present study avoids this dilemma by focusing on postformational mtDNA and allozyme mutations within a monophyletic lineage of the unisexual fish Poeciliopsis monacha-occidentalis (hereafter MO). The MO biotype arose in northwestern Mexico (Fig. 1A) via crosses be...

The origin and evolution of a unisexual hybrid:Poecilia formosa

“…The parthenogenetic grasshopper Warramaba virgo was estimated to be ca 300 000 years old (Kearney et al 2006). In unisexual fishes (Poeciliopsis complex), mtDNA variability was high indicating a rather ancient origin (Quattro et al 1992). Similar results were found in parthenogenetic geckos (Moritz & Heideman 1993;Kearney et al 2006).…”

“…They are often assessed as evolutionary 'dead ends' (Bell 1982). Many species, however, are rather abundant, show large ranges of geographical distribution and have shown to be evolutionary older than predicted from theoretical models (Quattro et al 1992;Schartl et al 1995b;Kearney et al 2006).…”

High male incidence and evolutionary implications of triploid form in northeast Asia Carassius auratus complex

“…However, most of unisexual vertebrates, such as kleptogenetic Ambystoma salamanders (Bi and Bogart, 2010;Spolsky et al, 1992), hybridogenetic Poeciliopsis fish (Quattro et al, 1992), gynogenetic Amazon molly (Lampert and Schartl, 2008;Schartl et al, 1995), Phoxinus eosneogaeus hybrids (Angers and Schlosser, 2007), and gynogenetic Cobitis (Janko et al, 2003), have been revealed to have long history and large ranges of geographical distribution (Avise, 2008). And, high genetic diversity has been extensively observed in gynogenetic or hybridogenetic fish (Angers and Schlosser, 2007;Cunha et al, 2011;Schmidt et al, 2011;Stöck et al, 2012), kleptogenetic amphibians (Bi and Bogart, 2010) and parthenogenetic reptiles (Fujita et al, 2007;Kupriyanova, 2009).…”

Character displacement in sailfin mollies, Poecilia latipinna: allozymes and behavior

“…Poeciliopsis divided about 8-16 million years ago (Mateos & Vrijenhoek 2002). The hybridogen, Poeciliopsis monacha-occidentalis based on mitochondrial evidence may be 150,000 years old (Quattro et al 1992) and lives throughout Sonora, Mexico and mates with males of the sexual species P. occidentalis. A similar history may hold for Amazon mollies.…”