Laboratory synthesis of an independently reproducing vertebrate species

Abstract

Speciation in animals commonly involves an extrinsic barrier to genetic exchange followed by the accumulation of sufficient genetic variation to impede subsequent productive interbreeding. All-female species of whiptail lizards, which originated by interspecific hybridization between sexual progenitors, are an exception to this rule. Here, the arising species instantaneously acquires a novel genotype combining distinctive alleles from two different species, and reproduction by parthenogenesis constitutes an effective intrinsic barrier to genetic exchange. Fertilization of diploid parthenogenetic females by males of sexual species has produced several triploid species, but these instantaneous speciation events have neither been observed in nature nor have they been reconstituted in the laboratory. Here we report the generation of four self-sustaining clonal lineages of a tetraploid species resulting from fertilization of triploid oocytes from a parthenogenetic Aspidoscelis exsanguis with haploid sperm from Aspidoscelis inornata. Molecular and cytological analysis confirmed the genetic identity of the hybrids and revealed that the females retain the capability of parthenogenetic reproduction characteristic of their triploid mothers. The tetraploid females have established self-perpetuating clonal lineages which are now in the third generation. Our results confirm the hypothesis that secondary hybridization events can lead to asexual lineages of increased ploidy when favorable combinations of parental genomes are assembled. We anticipate that these animals will be a critical tool in understanding the mechanisms underlying the origin and subsequent evolution of asexual amniotes.hybrid speciation | polyploidy | Cnemidophorus | unisexual

Morphological Variation in a Unisexual Whiptail Lizard (Aspidoscelis exsanguis) and One of Its Bisexual Parental Species (Aspidoscelis inornata) (Reptilia: Squamata: Teiidae): Is the Clonal Species Less Variable?

“…The two lineages of A. neavesi differed significantly in two characters, SPV and FP, although the actual differences were small (Cole et al, 2014). Nevertheless, the founders of those lineages were females from different F 1 hybrid zygotes of A. exsanguis × A. inornata (Lutes et al, 2011).…”

“…This preserves the high levels of heterozygosity that result from their hybrid origins (reviewed by Reeder et al, 2002) and explains their very low levels of variation in genetic characters, such as allozymes (e.g., Neaves, 1969;Parker and Selander, 1976;Dessauer and Cole, 1986;Taylor et al, 2015) and microsatellite DNA (Lutes et al, 2011). Nonlethal mutations can produce new or derived lineages of parthenogens, as they are cloned, so multiple clonal lineages can occur in populations of unisexual whiptail lizards (Parker and Selander, 1976;Dessauer and Cole, 1989;Lutes et al, 2011). Different clones can also result from separate original F 1 hybrid zygotes (e.g., Cole and Dessauer, 1993;Lutes et al, 2011).…”

“…Nonlethal mutations can produce new or derived lineages of parthenogens, as they are cloned, so multiple clonal lineages can occur in populations of unisexual whiptail lizards (Parker and Selander, 1976;Dessauer and Cole, 1989;Lutes et al, 2011). Different clones can also result from separate original F 1 hybrid zygotes (e.g., Cole and Dessauer, 1993;Lutes et al, 2011).…”

Spontaneous speciation by ploidy elevation: Laboratory synthesis of a new clonal vertebrate

“…In this context, the report by Lutes et al (5) in PNAS is highly significant. Following from an earlier observation of a potentially fertile, fieldcollected 4n female (7), Lutes et al (5) crossed parthenogenetic 3n Aspidoscelis exsanguis females and a sexual Aspidoscelis inornata male to produce three generations of parthenogenetically reproducing 4n female lizards. Parthenogenetic reproduction was confirmed by cytogenetic analysis of female meiosis and multilocus genotyping across multiple generations of the progeny.…”

What does the geography of parthenogenesis teach us about sex?

“…This diversity can be ancient and stem from several independent origins. Alternatively, the generation of new asexual genotypes can still be ongoing, for instance via mutation [64], continuing hybridization of, or with, the sexual parents [65], contagious asexuality via endosymbiont transmission [66] or rare crossings with sexuals (e.g. [42] in hermaphrodite flatworms; [67] in Daphnia and [68] in Artemia owing to rare parthenogenetic sons), or forms of 'parasex' [69] such as horizontal gene transfer between individuals (bdelloid rotifers, see [70]) or introgression of environmental DNA (anhydrobiotic rotifers or tardigrades [71]).…”