Resolving complex phylogeographic patterns in the Balkan Peninsula using closely related wall-lizard species as a model system

Psonis, Nikolaos; Antoniou, Aglaia; Karameta, Emmanouela; Leaché, Adam D.; Kotsakiozi, Panayiota; Darriba, Diego; Kozlov, Alexey M; Stamatakis, Alexandros; Poursanidis, Dimitris; Kukushkin, Oleg V.; Jablonski, Daniel; Crnobrnja‐Isailović, Jelka; Gherghel, Iulian; Lymberakis, Petros

doi:10.1016/j.ympev.2018.03.021

Cited by 33 publications

(61 citation statements)

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“…1B and 1C). Subsequently in the Late Pleistocene, E. sauromates s. s. reoccupied the territories of eastern Europe concomitant with dispersing north of the steppe and semi-desert habitats and the Black Sea regression (Ratnikov, 2014), similarly as proposed for the snake Dolichophis caspius (Nagy et al, 2010) and lizards Lacerta viridis (Marzahn et al, 2016), Pseudopus apodus (Jandzik et al, 2018), and Podarcis tauricus (Psonis et al, 2018). Before the terminal phase of the last Pleistocene glaciation, E. sauromates already lived in the Crimean Mountains as confirmed by the fossil record (Ratnikov, 2015), although remnants of E. quatuorlineata–sauromates from the Pleistocene and Holocene are not known from the East European Plain (Ratnikov, 2002).…”

Section: Discussionmentioning

confidence: 76%

The biogeography ofElaphe sauromates(Pallas, 1814), with a description of a new rat snake species

Jablonski

Kukushkin

Avcı

et al. 2019

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Background The rat snake genus Elaphe once comprised several dozens of species distributed in temperate through tropical zones of the New and Old World. Based on molecular-genetic analyses in early 2000s, the genus was split into several separate genera, leaving only 15 Palearctic and Oriental species as its members. One of the three species also occurring in Europe is Elaphe sauromates, a robust snake from the Balkans, Anatolia, Caucasus, Ponto-Caspian steppes, and Levant that has been suspected to be composed of two or more genetically diverse populations. Here, we studied the genetic structure and morphological variation of E. sauromates, aiming to better understand its inter-population relationships and biogeography, and subsequently revise its taxonomy. Methods We reconstructed the phylogeography and analyzed the genetic structure of E. sauromates populations originating from most of its geographic range using both mitochondrial (COI, ND4) and nuclear (C-MOS, MC1R, PRLR, RAG1) DNA gene fragments. We employed Maximum likelihood and Bayesian inference methods for the phylogenetic tree reconstructions, supplemented with species delimitation methods, analysis of haplotype networks, and calculation of uncorrected p-distances. Morphological variation in 15 metric and 18 meristic characters was studied using parametric univariate tests as well as multivariate general linearized models. In total, we analyzed sequences originating from 63 specimens and morphological data from 95 specimens of E. sauromates sensu lato. Results The molecular phylogeny identified two clearly divergent sister lineages within E. sauromates, with both forming a lineage sister to E. quatuorlineata. The genetic distance between them (5.80–8.24% in mtDNA) is similar to the distances among several other species of the genus Elaphe. Both lineages are also moderately morphologically differentiated and, while none of the characters are exclusively diagnostic, their combination can be used for confident lineage identification. Here, following the criteria of genetic and evolutionary species concepts, we describe the lineage from eastern Anatolia and parts of the Lesser and Great Caucasus as a new species E. urartica sp. nov. Discussion Elaphe urartica sp. nov. represents a cryptic species whose ancestors presumably diverged from their common ancestor with E. sauromates around the Miocene-Pliocene boundary. The intraspecific genetic structure indicates that the recent diversity of both species has been predominantly shaped by Pleistocene climatic oscillations, with glacial refugia mainly located in the Balkans, Crimea, and/or Anatolia in E. sauromates and Anatolia and/or the Caucasus in E. urartica sp. nov.

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Section: Discussionmentioning

confidence: 76%

The biogeography ofElaphe sauromates(Pallas, 1814), with a description of a new rat snake species

Jablonski

Kukushkin

Avcı

et al. 2019

PeerJ

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“…The revolution initiated by high-throughput sequencing techniques has reached the field of phylogeography (Coates et al 2018), where it lifts the veil on cryptic species and solves long-term taxonomic issues (e.g. Rodriguez et al 2017; Psonis et al 2018; Dufresnes et al 2018, 2019a). We conducted such study in spadefoot toads from the monotypic family Pelobatidae Bonaparte, 1850 (genus Pelobates Wagler, 1830) endemic to the Western Palearctic (Dufresnes et al 2019b).…”

Section: Introductionmentioning

confidence: 99%

Call a spade a spade: taxonomy and distribution of Pelobates, with description of a new Balkan endemic

Dufresnes¹,

Strachinis²,

Tzoras³

et al. 2019

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The genomic era contributes to update the taxonomy of many debated terrestrial vertebrates. In an accompanying work, we provided a comprehensive molecular assessment of spadefoot toads (Pelobates) using genomic data. Our results call for taxonomic updates in this group. First, nuclear phylogenomics confirmed the species-level divergence between the Iberian P.cultripes and its Moroccan relative P.varaldii. Second, we inferred that P.fuscus and P.vespertinus, considered subspecies until recently, feature partial reproductive isolation and thus deserve a specific level. Third, we evidenced cryptic speciation and diversification among deeply diverged lineages collectively known as Pelobatessyriacus. Populations from the Near East correspond to the Eastern spadefoot toad P.syriacus sensu stricto, which is represented by two subspecies, one in the Levant (P.s.syriacus) and the other in the rest of the range (P.s.boettgeri). Populations from southeastern Europe correspond to the Balkan spadefoot toad, P.balcanicus. Based on genetic evidence, this species is also polytypic: the nominal P.b.balcanicus inhabits the Balkan Peninsula; a new subspecies P.b.chloeaessp. nov. appears endemic to the Peloponnese. In this paper, we provide an updated overview of the taxonomy and distribution of all extant Pelobates taxa and describe P.b.chloeaessp. nov.

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“…The high genetic diversity reported here, along with that observed in other phylogeographic studies, places the Tyrrhenian wall lizard among those species characterized by high genetic diversity regardless of its relatively small distribution (Ketmaier & Caccone, and references therein; Salvi et al ., ). Within Podarcis , such a high intraspecific differentiation is only comparable to some continental species such as P. siculus , P. muralis and P. tauricus (Salvi et al ., ; Psonis et al ., , ; Senczuk et al ., ). Although Corsica and Sardinia are geographically less complex than mainland Europe, most of the examined species showed complex responses to the Pleistocene climate oscillations.…”

Section: Discussionmentioning

confidence: 97%

The role of island physiography in maintaining genetic diversity in the endemic Tyrrhenian wall lizard (Podarcis tiliguerta)

et al. 2019

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Sea level oscillations occurred during the Pleistocene have strongly affected islands’ physiography by changing area, elevation, and even the number of islands rising above the sea level. Such changes had direct consequences on island genetic diversity by promoting genetic admixture during glacial marine regressions while fragmentation or even extinctions occurred because of marine transgressions. Here we investigated the effect of islands’ physiographic changes on the mitochondrial diversity of 84 individuals of the Tyrrhenian wall lizard (Podarcis tiliguerta) from different islands and island groups surrounding Corsica and Sardinia. The La Maddalena Archipelago that is the more complex of the studied island groups, showed the highest genetic diversity, while we detected decreasing genetic diversity in island groups with lower number of islands and elevation. The genetic imprint we found seems to have been shaped by eustatic changes occurred in the Mediterranean basin during Mid‐Pleistocene times. Indeed, a relevant component of ancient lineages was found on those island groups among which elevation of at least one island allowed populations to survive during the Mid‐Pleistocene marine transgressions. In contrast, we found evidence of recent gene flow between populations inhabiting islands or island groups characterized by low elevation. Our results suggest that many features such as number of islands and their elevation, may provide predictive information to identify those islands or “archipelagos” that deserve special attention in terms of conservation priority.

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Resolving complex phylogeographic patterns in the Balkan Peninsula using closely related wall-lizard species as a model system

Cited by 33 publications

References 116 publications

The biogeography ofElaphe sauromates(Pallas, 1814), with a description of a new rat snake species

The biogeography ofElaphe sauromates(Pallas, 1814), with a description of a new rat snake species

Call a spade a spade: taxonomy and distribution of Pelobates, with description of a new Balkan endemic

The role of island physiography in maintaining genetic diversity in the endemic Tyrrhenian wall lizard (Podarcis tiliguerta)

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