Multiple interspecific hybridization and microsatellite mutations provide clonal diversity in the parthenogenetic rock lizard Darevskia armeniaca

Abstract

BackgroundThe parthenogenetic Caucasian rock lizard Darevskia armeniaca, like most other parthenogenetic vertebrate species, originated through interspecific hybridization between the closely related sexual Darevskia mixta and Darevskia valentini. Darevskia armeniaca was shown to consist of one widespread allozyme clone and a few rare ones, but notwithstanding the origin of clonal diversity remains unclear. We conduct genomic analysis of D. armeniaca and its parental sexual species using microsatellite and SNP markers to identify the origin of parthenogenetic clonal lineages.ResultsFour microsatellite-containing loci were genotyped for 111 specimens of D. armeniaca, 17 D. valentini, and four D. mixta. For these species, a total of 47 alleles were isolated and sequenced. Analysis of the data revealed 13 genotypes or presumptive clones in parthenogenetic D. armeniaca, including one widespread clone, two apparently geographically restricted clones, and ten rare clones. Comparisons of genotype-specific markers in D. armeniaca with those of its parental species revealed three founder-events including a common and two rare clones. All other clones appeared to have originated via post-formation microsatellite mutations in the course of evolutionary history of D. armeniaca.ConclusionOur new approach to microsatellite genotyping reveals allele-specific microsatellite and SNP markers for each locus studied. Interspecies comparison of these markers identifies alleles inherited by parthenospecies from parental species, and provides new information on origin and evolution of clonal diversity in D. armeniaca. SNP analyses reveal at least three interspecific origins of D. armeniaca, and microsatellite mutations in these initial clones give rise to new clones. Thus, we first establish multiple origins of D. armeniaca. Our study identifies the most effective molecular markers for elucidating the origins of clonal diversity in other unisexual species that arose via interspecific hybridization.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5359-5) contains supplementary material, which is available to authorized users.

Genotypic similarities among the parthenogenetic Darevskia rock lizards with different hybrid origins

“…Discussion of the origins of parthenogenetic Darevskia usually posits several background premises: (1) each of seven parthenogenetic forms of Darevskia derives from independent hybridization events [ 32 , 33 , 54 , 55 ]; (2) the parental species of the extant parthenogens belong to different clades within Darevskia [ 36 , 37 , 45 ]; (3) high heterozygosity of the parthenogens derives from their hybrid origin; (4) all extant parthenogenetic lineages originated in relatively recent geological past, i.e. within the last 200,000 years [ 32 , 36 ]; (5) genetic exchange between parthenogenetic lineages and sexually reproducing Darevskia is rare or nonexistent [ 32 , 37 , 61 , 72 ].…”

“…Tarkhnishvili et al [ 24 ] found two heterozygous single-locus genotypes (at Du47 and Du323) shared at high frequencies in both D. armeniaca and D. dahli . Vergun et al [ 54 ] and Girnyk et al [ 55 ] genotyped 111 specimens of D. dahli and 111 D. armeniaca from Armenia using four out of the ten loci included in our analysis (Du215, Du281, Du323, and Du47). Comparing the data between these two studies, the heterozygous genotype comprised of alleles 184 and 211 at the locus Du323 was shared by nearly all specimens of D. armeniaca (0.94) and one-third of D. dahli (0.27).…”

“…Potentially, one could explain polymorphism within the parthenogens by the aggregation of de novo mutations. However, additional evidence caused multiple authors to interpret genetic variation within the parthenogens as polyclonality, i.e., descent from different F1 hybrids [ 48 , 49 , 51 , 52 , 54 , 55 ]; but see [ 53 ]. In our study, the presence of multiple and fixed differences between D. armeniaca and D. dahli is probably not solely the result of accumulated mutation; at least such extent of divergent phenotypic evolution is unknown in vertebrate parthenogens.…”

“…Polymorphisms were also recorded for D. armeniaca [ 36 , 49 , 50 ], D. dahli [ 51 , 52 ], D. unisexualis [ 37 , 48 ], D. rostombekowi [ 53 ], D. uzzelli and D. bendimahiensis [ 48 ]. Vergun et al [ 54 ], Ryskov et al [ 53 ], and Girnyk et al [ 55 ] examined the nucleotide sequence variation in amplicons containing the microsatellite repeats, in D. dahli , D. rostombekowi , and D. armeniaca . The variation in the repeat lengths at individual loci was attributed to mutations within the clonal parthenogenetic lineages, while the single-nucleotide variants in the regions flanking the repeats were assumed to be due to independent hybridization events.…”

Species Distribution Models and Niche Partitioning among Unisexual Darevskia dahli and Its Parental Bisexual (D. portschinskii, D. mixta) Rock Lizards in the Caucasus

“…For this reason, FNV model suggests that bisexual species are not able to co-exist with a large number of parthenogenetic lineages which can suppress them [92][93][94]. This finding is supported by the fact that D. mixta was excluded from its native range by a large number of clones of D. armeniaca and D. dahli [23,95]. It is noteworthy that D. mixta is the only "maternal" species of the genus Darevskia that competed with multiple parethenogenetic clones of D. armeniaca and D. dahli simultaneously, since niche elevation centroid of D. mixta is located at the intermediate position between centroids of D. armeniaca (top) [31] and D. dahli (bottom).…”