Cytochrome b mitochondrial gene analysis-based phylogeography of a Sand lizard in the Crimea: ancient refugium at the peninsula, late expansion from the North, and first evidence of Lacerta agilis tauridica and L. a. exigua (Lacertidae: Sauria) hybridization

Abstract

The contact zones of the distribution ranges of closely related reptile taxa are the source of valuable data on the microevolutionary processes in populations, the history of regional faunas origin, and the environmental preferences of the studied forms. Our study is focused on the genetic structure of the populations of sand lizard, Lacerta agilis Linnaeus, 1758, at the Crimean peninsula. This lacertid species inhabits the mountain (afforested) and plain (steppe) parts of the Crimea, being abundant or common in many areas. Lacerta agilis is represented in the Crimea by two subspecies: the widely distributed Eastern (L. a. exigua Eichwald, 1831) inhabiting a large part of Northern Eurasia, and the endemic (L. a. tauridica Suchow, 1927) residing in the Crimean mountains. Mitochondrial haplogroup affiliation corresponding to one of the subspecies (L. a. tauridica, L. a. exigua or L. a. chersonensis) was established for 225 L. agilis individuals from 81 localities in the Crimea and adjacent mainland territories. The nucleotide sequences of the complete cytochrome b gene of mitochondrial DNA (1143 bp) were studied in 75 L. agilis individuals from 68 localities. The genetic distance between both subspecies inhabiting the Crimea revealed by used molecular marker comprised 2.8%, which indicates their early divergence approximately at the transition of Early to Middle Pleistocene (ca. 1 Mya). L. a. tauridica is characterized by a comparatively deep genetic structure. Haplotypes occupying isolated positions on the phylogenetic tree of this subspecies were found in the south-western part of the Crimean Mountains, what might be explained by the localization of L. agilis microrefugia in areas least affected by the Late Pleistocene cooling. Genetic structure of L. a. exigua is more homogeneous. Another important result of our study was an identification of zones of haplogroups «exigua» and «tauridica» coexistence localized along the northern and eastern margins of the Crimean Mountains. The portion of the «exigua» haplogroup in local populations decreases southward and westward. The observed pattern of the spatial distribution of haplogroups seems to be a result of the hybridization zone formation between the sand lizard subspecies during the Holocene expansion of L. a. exigua. Ecological niches modeling for L. agilis subspecies and analysis of morphological variability of the lizards support the hypothesis of L. a. exigua and L. a. tauridica hybridization in the area of contact of their ranges in the eastern part of the Crimean Mountains.

The mitochondrial phylogeography of the Crimean endemic lizard Darevskia lindholmi (Sauria, Lacertidae): Hidden diversity in an isolated mountain system

“…Thus, the level of endemism here is low, and unique genetic di versity (though only slightly different from the mainland populations) was detected only for few vertebrate species, especially reptiles (Fritz et al 2009;Zinenko et al 2015;Psonis et al 2017Psonis et al , 2018Jablonski et al 2019). In addi tion to the Crimean member of the genus Darevskia, the only endemic reptile taxon to the Crimean Mountains is Lacerta agilis tauridica Suchow, 1927, whose morpho logical uniqueness was supported also by genetic data (Joger et al 2007;Andres et al 2014;Kukushkin et al 2020). Lacerta viridis magnifica Sobolevssky, 1930, for mer endemic subspecies of Lacertidae from Crimea, was identified as an introduced, currently extinct population of L. bilineata (Kehlmaier et al 2020).…”

“…The closest ancestral haplo types of D. lindholmi represented by the Southwestern lineage probably persisted in the extreme south of Crimea (potential refugium), where the influence of climatic os cillations was less pronounced (Gerasimenko 2007(Gerasimenko , 2011Pisareva et al 2019). A similar pattern is expected for the Crimean montane subspecies of L. agilis (Kukushkin et al 2020). The subsequent population divergence of D. lindholmi could thus correspond with landscape and climatic changes or niche differentiation (see below).…”

The first comprehensive data on the distribution of reptiles within the Southern Bug eco-corridor, Ukraine

“…Fritz et al 2009;Guicking et al 2009;Musilova et al 2010;Poyarkov et al 2014;Zinenko et al 2015;Marzahn et al 2016;Psonis et al 2018;Jablonski et al 2019a, b). However, the North Black Sea region may also be a potential source of local genetic diversity for at least some reptile species (see Kukushkin et al 2020;Mahtani-Williams et al 2020).…”

Environment drives color pattern polymorphism in sand lizards beyond the Gloger's rule

“…to 60.4° N in Southern Scandinavia (Agasyan et al., 2021). Sand lizards have 10 subspecies with additional color and color pattern variation that does not correspond to the subspecies (Bischoff, 1984; Kukushkin et al., 2020; Nekrasova et al., 2018). The sand lizard color fluctuates seasonally, ontogenetically, and differs between sexes (Edgar & Bird, 2006), but color pattern is more stable, varying primarily with ontogeny.…”