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Öğe Disentangling population genetic and climatic effects on skull size and shape of brown hares, Lepus europaeus (Lagomorpha: Leporidae), from Turkiye(Elsevier Gmbh, 2023) Demirbas, Yasin; Koca, Ayca Ozkan; Stefanovic, Milomir; Smith, Steve; Suchentrunk, FranzBrown hares (Lepus europaeus) from Turkiye exhibit substantial phenotypic variation, assumingly connected to regional climate differences. We used general linear models (GLMs) of linear measurements and geometric morphometric data of dorsal and ventral skull and lateral mandible landmarks of 160 adult individuals from 75 locations across Turkiye, to specifically test for climate-related effects on skull size and shape, while accounting for potentially confounding effects of sex, geographic location, and population genetic assignment. We found a moderate positive correlation between individual condylobasal lengths (CBL) and centroid size scores (CSS) and used them separately as dependent skull size variables in our GLMs. Skull shape factors were obtained from principal component analyses (PCAs), separately for transformed linear morphometric and landmark data; they were also used as dependent variables in our GLMs, along with sex, geographic sampling coordinates, CBL or CSS, as well as temperature and precipitation factors from PCAs of local climate data as fixed factors. Our multivariate GLMs returned no climate effect on skull size and only one minor precipitation effect on geometric skull shape. Rather, skull size and shape were predominantly and significantly affected by the assignment of the hares to the genetic populations as determined by an earlier microsatellite study. Our results correspond to microphylogeographic differentiation of skull size and shape of the studied hares, largely indepedent of specific adaptation to local or regional climate.Öğe Positive selection and precipitation effects on the mitochondrial NADH dehydrogenase subunit 6 gene in brown hares (Lepus europaeus) under a phylogeographic perspective(Public Library Science, 2019) Stefanovic, Milomir; Djan, Mihajla; Velickovic, Nevena; Beukovic, Dejan; Lavadinovic, Vukan; Zhelev, Chavdar DinevPrevious studies in hares and jackrabbits have indicated that positive selection has shaped the genetic diversity of mitochondrial genes involved in oxidative phosphorylation, which may affect cellular energy production and cause regional adaptation to different environmental (climatic) pressures. In the present study, we sequenced the NADH dehydrogenase subunit 6 (MT-ND6) gene of 267 brown hares (L. europaeus) from Europe and Asia Minor and tested for positive selection and adaptations acting on amino acid sequences (protein variants). Molecular diversity indices and spatial clustering were assessed by DnaSP, Network, and Geneland, while the presence of selection signals was tested by codeml in PAML, and by using the Datamonkey Adaptive Evolution web server. The SPSS software was used to run multinomial regression models to test for possible effects of climate parameters on the currently obtained protein variants. Fifty-eight haplotypes were revealed with a haplotype diversity of 0.817, coding for 17 different protein variants. The MT-ND6 phylogeographic pattern as determined by the nucleotide sequences followed the earlier found model based on the neutrally evolving D-loop sequences, and reflected the earlier found phylogeographic Late Pleistocene scenario. Based on several selection tests, only one codon position consistently proved to be under positive selection. It did occur exclusively in the evolutionarily younger hares from Europe and it gave rise to several protein variants from the southeastern and south-central Balkans. The occurrence of several of those variants was significantly favored under certain precipitation conditions, as proved by our multinomial regression models. Possibly, the great altitudinal variation in the Balkans may have lead to bigger changes in precipitation across that region and this may have imposed an evolutionarily novel selective pressure on the protein variants and could have led to regional adaptation.Öğe Purifying selection shaping the evolution of the Toll-like receptor 2 TIR domain in brown hares (Lepus europaeus) from Europe and the Middle East(SPRINGER, 2020) Stefanovic, Milomir; Djan, Mihajla; Velickovic, Nevena; Demirbas, Yasin; Paule, Ladislav; Gedeon, Csongor Istvan; Posautz, AnnikaToll-like receptors (TLRs) are transmembrane proteins of the innate immune system, composed of the ectodomain involved in pathogen recognition and the intracellular Toll/interleukin-1 receptor (TIR) domain important for downstream signal transduction. Here, we analyze the genetic variability of TIR nucleotide and amino-acid sequences of the TLR2 gene in 243 brown hares from Europe and the Middle East and tested for the presence of selection signals and spatial structuring. TLR2 TIR domain sequences were PCR amplified and sequenced, while genotyping was performed by phasing. Genetic diversity indices were calculated in DnaSP and Arlequin, while presence of selection signals was tested using MEGA and the Datamonkey web server. The presence of spatial patterns in TIR sequence distribution was tested by spatial Principal Component Analysis (sPCA) in adegenet. A total of 13 haplotypes were revealed with haplotype diversity of 0.424, and nucleotide diversity (pi) of 0.00138. Two spatial clusters were revealed: "Anatolia/Middle East" and "Europe". In Anatolia the two most prevalent amino-acid variants, A and B (the latter being the most ancestral) were maintained at similar frequencies; but in Europe a shift in genotype frequencies was observed as well as a higher number of nonsynonymous substitutions giving rise to novel amino-acid protein variants originating from the evolutionarily younger protein variant. Molecular diversity (haplotype and nucleotide diversity) indices were significantly higher in the "Anatolia/Middle East" cluster. A signal of purifying selection was detected acting on the TIR sequences.Öğe Spatial genetics of brown hares (Lepus europaeus Pallas, 1778) from Turkey: Different gene pool architecture on either side of the Bosphorus?(Elsevier Gmbh, 2019) Demirbas, Yasin; Albayrak, Irfan; Koca, Ayca Ozkan; Stefanovic, Milomir; Knauer, Felix; Suchentrunk, FranzWe determined allelic variation at eleven microsatellite loci to study the effect of the Bosphorus, the Sea of Marmara, and the Dardanelles on the population genetic architecture of brown hares, Lepus europaeus, from Anatolia and Turkish Thrace in the southeastern most Balkans. The latter region was connected with Anatolia during periods of the late Pleistocene and the early Holocene (until ca. 8000 y BP) enabling natural gene flow. Following a recent mitochondrial (mt) DNA-based phylogeographic model that suggested unidirectional ancient gene flow from Anatolia to the SE Balkans, we expected lower genetic diversity in hares from Turkish Thrace than Anatolia. The Turkish Thrace population might have been established only relatively recently as natural northwestward expansion of a long existing Anatolian population. Alternatively, it might have received late Pleistocene or Holocene gene flow by hares from eastern Europe from north of the Black Sea, even after the formation of the marine barrier. This might have produced a notable genetic distinction between the hares from either side of the Bosphorus, the Sea of Marmara, and the Dardanelles. We found significantly lower allelic richness in hares from Turkish Thrace than Anatolia, very little genetic admixture in the Turkish Thrace population, and only one allele at low frequency in Turkish Thrace that was not observed in Anatolian hares. On the contrary, many alleles of Anatolian hares were not recovered in hares from Turkish Thrace. Nevertheless, genetic divergence (Fst, Cavalli-Sforza & Edwards distances, AMOVA) between the hares from either side of the current marine barrier was low (Fst values <10%). All findings accord to our initial hypothesis that the hares from Turkish Thrace represent merely a somewhat genetically depleted version of the Anatolian hares. Seemingly, no strong drift has occurred in the Turkish Thrace population since the break-up of the Holocene landbridge, and there is no indication of gene flow from other regions in (eastern) Europe into the Turkish Thrace population. Spatial genetic approaches and standard population genetics (BAPS, GENELAND, STRUCTURE, F-statistics, Cavalli-Sforza & Edwards distances) indicated significant spatial genetic differentiation of hares across Anatolia, but also on a very low level. Overall, our results are concordant with the latest mtDNA based model of ancient gene flow in hares only from Anatolia to the southeastern Balkans across the Pleistocene and early Holocene landbridge; this implies that most or all of the Balkans have been colonized by hares exclusively originating eventually from Anatolia. (C) 2018 Deutsche Gesellschaft fur Saugetierkunde. Published by Elsevier GmbH. All rights reserved.
