Tanja D. Vukov

Tracing glacial refugia of Triturus newts based on mitochondrial DNA phylogeography and species distribution modeling

IntroductionThe major climatic oscillations during the Quaternary Ice Age heavily influenced the distribution of species and left their mark on intraspecific genetic diversity. Past range shifts can be reconstructed with the aid of species distribution modeling and phylogeographical analyses. We test the responses of the different members of the genus Triturus (i.e. the marbled and crested newts) as the climate shifted from the previous glacial period (the Last Glacial Maximum, ~21 Ka) to the current interglacial.ResultsWe present the results of a dense mitochondrial DNA phylogeography (visualizing genetic diversity within and divergence among populations) and species distribution modeling (using two different climate simulations) for the nine Triturus species on composite maps.ConclusionsThe combined use of species distribution modeling and mitochondrial phylogeography provides insight in the glacial contraction and postglacial expansion of Triturus. The combined use of the two independent techniques yields a more complete understanding of the historical biogeography of Triturus than both approaches would on their own. Triturus newts generally conform to the ‘southern richness and northern purity’ paradigm, but we also find more intricate patterns, such as the absence of genetic variation and suitable area at the Last Glacial Maximum (T. dobrogicus), an ‘extra-Mediterranean’ refugium in the Carpathian Basin (T. cristatus), and areas where species displaced one another postglacially (e.g. T. macedonicus and western T. karelinii). We provide a biogeographical scenario for Triturus, showing the positions of glacial refugia, the regions that were postglacially colonized and the areas where species displaced one another as they shifted their ranges.

Nuclear and mitochondrial phylogeography of the European fire-bellied toads Bombina bombina and Bombina variegata supports their independent histories

Exact location and number of glacial refugia still remain unclear for many European cold‐blooded terrestrial vertebrates. We performed a fine‐scaled multilocus phylogeographic analysis of two Bombina species combining mitochondrial variation of 950 toads from 385 sites and nuclear genes (Rag‐1, Ncx‐1) from a subset of samples to reconstruct their colonization and contemporary variation patterns. We identified the lowlands northwest of the Black Sea and the Carpathians to be important refugial areas for B. bombina and B. variegata, respectively. This result emphasizes the importance of Central European refugia for ectothermic terrestrial species, far north of the Mediterranean areas regarded as exclusive glacial refugia for the animals. Additional refugia for B. variegata have been located in the southern Apennines and Balkans. In contrast, no evidence for the importance of other east European plains as refugial regions has been found. The distribution of mtDNA and Ncx‐1 variation suggests the presence of local refugia near the Black Sea for B. bombina; however, coalescent simulations did not allow to distinguish whether one or two refugia were present in the region. Strong genetic drift apparently accompanied postglacial expansions reducing diversity in the colonization areas. Extended sampling, coupled with the multilocus isolation with migration analysis, revealed a limited and geographically restricted gene flow from the Balkan to Carpathian populations of B. variegata. However, despite proximity of inferred B. bombina and B. variegata refugia, gene exchange between them was not detected.

Ontogeny of skull size and shape changes within a framework of biphasic lifestyle: a case study in six Triturus species (Amphibia, Salamandridae)

As with many other amphibians, Triturus species are characterized by a biphasic life cycle with abrupt changes in the cranial skeleton during metamorphosis. The post-metamorphic shape changes of the cranial skeleton were investigated using geometric morphometric techniques in six species: Triturus alpestris, T. vulgaris, T. dobrogicus, T. cristatus, T. carnifex, and T. karelinii. The comparative analysis of ontogenetic trajectories revealed that these species have a conserved developmental rate with divergent ontogenetic trajectories of the ventral skull shape that mainly reflect phylogenetic relatedness. A striking exception in the ontogenetic pattern was possibly found in T. dobrogicus, characterized by a marked increase in the developmental rate compared to the other newt species. The size-related shape changes explained a large proportion of shape change during post-metamorphic growth within each species, with marked positive allometric growth of skull elements related to foraging.

Distribution patterns and environmental determinants of European newts in the Montenegrin karst area

The distribution patterns of three European newt species (Triturus macedonicus, Lissotriton vulgaris, and Mesotriton alpestris) was determined in the Montenegrin karst region and the influence of breeding ponds, the adjacent landscape, and climate variables on distributions within the framework of allotopy vs. syntopy occurrences was tested. After surveying 145 newt breeding sites in a 10,080 km2 area, the ranges of T. macedonicus and M. alpestris were found not come into contact, while L. vulgaris, the most widely distributed species, covers the entire range of T. macedonicus and the lower part of the range of M. alpestris. Using Akaike’s Information Criterion (AIC) to evaluate the effectiveness of 70 a priori models in predicting the presence of the three newt species, it was found that: (1) elevation is the most important variable in predicting newt presence; (2) only a few elevation-dependent variables can replace elevation in the building of a good descriptive model; (3) precipitation in combination with elevation contributes significantly to the building of a better descriptive model; and (4) in comparison with allotopy, syntopy mostly occurs at intermediate elevation ranges of species in sympatry.

The study of larval tail morphology reveals differentiation between two Triturus species and their hybrids

In amphibians, morphological differentiation and disparity at the larval and post-metamorphic ontogenetic stages can diverge, owing to various contrasting environments and different selective pressures. In the monophyletic clade of nine Triturus newt species, five different morphotypes can be recognized, but information on larval morphology is limited. Here we explore divergence of larval morphology in Triturus ivanbureschi , T. macedonicus , and their F1 hybrids. These two genetically and morphologically distinct crested newt species hybridize in nature and form a relatively wide hybrid zone in the central part of the Balkan Peninsula. Using a geometric morphometric approach and multivariate statistics, we evaluated differences of tail size and shape, colouration pattern, and the presence of a tail filament at the mid-larval stage in larvae reared under controlled laboratory conditions. We chose the tail as the main propulsive organ crucial for locomotion, feeding, and escaping predators. We found that Triturus ivanbureschi and T. macedonicus larvae differ in tail shape, but not in tail size. Two groups of F1 hybrid larvae (obtained from reciprocal crossing) were similar to each other, but differed from the parental species in size and shape of the tail, colouration pattern, and the presence of a tail filament. Our results indicate that, like adults, larvae diverge morphologically and hybrid larvae do not exhibit intermediate morphology of the parental species.

The Roles of Phylogeny and Climate in Shaping Variation in Life-History Traits of the Newt Genus Triturus (Caudata, Salamandridae)

Assessing the origin of trait variation during evolutionary history is an important first step in understanding evolutionary diversification. Here, we tested the influence of shared ancestry and climate, and the interplay of both, on the variation of ten life history traits in Triturus newts. We showed that (1) climate alone has driven the evolution of variation in five life history traits, (2) phylogenetic signal partly explains the variation in two traits (vitellus diameter and snout—vent length of larvae at metamorphosis), and (3) the interplay of shared ancestry and climate explains the variation in one trait (snout—vent length of larvae at metamorphosis). This study highlights the coarse-grained influence of shared ancestry and climate on the structure of phenotypic trait variation in Triturus and provides a handle for more detailed, fine grained studies on the evolution of phenotypic trait variation.

The geometric morphometrics and condition of Pontic shad, Alosa immaculata (Pisces: Clupeidae) migrants to the Danube River

Anadromous fish could have intraspecific groups with different life histories; identification of these is very important for management and conservation. Geometric morphometrics represents a quick and cost-effective method to identify such intraspecific groups. In this study, geometric morphometrics of Pontic shad (Alosa immaculata) migrants from the Danube River were investigated, as was Fultons condition factor (K), hepatosomatic index (HSI) and gonadosomatic index (GSI). Pontic shad specimens were collected during April and May of 2004 and 2006. The sample comprised four groups (65 males and 56 females in 2004; 110 males and 78 females in 2006). Geometric morphometrics revealed differences in shape that were statistically significant for both year (nested analysis of variance: F = 13.84; p < 0.001) and sex (nested analysis of variance: sex nested in year, F = 1.71; p < 0.01). The major differences between years were in head shape and position of fins. The most significant difference between females and males was in the dorsolateral expansion of the mid-body section with emphasis on the higher dorsal part of the body. Values for K in this work (0.65–0.70) were the lowest recorded for Pontic shad in the Danube River. Additional investigations involving both geometric morphometrics and molecular genetics are necessary to confirm the presence of races. This could be important information for conservation purposes as Pontic shad is listed as Vulnerable on the International Union for Conservation of Nature list.

The modular organization of roe deer (Capreolus capreolus) body during ontogeny: the effects of sex and habitat

BackgroundAs a small artiodactyl, the roe deer (Capreolus capreolus L.) is characterized by biological plasticity and great adaptability demonstrated by their survival under a wide variety of environmental conditions. In order to depict patterns of phenotypic variation of roe deer body this study aims to quantify variation during ontogenetic development and determine how sex-specific reproductive investment and non-uniform habitat differences relate to phenotypic variation and do these differential investments mold the patterns of phenotypic variation through modular organisation.ResultsPatterns of phenotypic correlation among body traits change during the ontogeny of roe deer, with differential influence of sex and habitat type. Modularity was found to be a feature of closed habitats with trunk+forelimbs+hindlimbs as the best supported integration/modularity hypothesis for both sexes. The indices of integration and evolvability vary with habitat type, age and sex where increased integration is followed by decreased evolvability.ConclusionThis is the first study that quantifies patterns of correlation in the roe deer body and finds pronounced changes in correlation structure during ontogeny affected by sex and habitat type. The correlation structure of the roe deer body is developmentally written over the course of ontogeny but we do not exclude the influence of function on ontogenetic changes. Modularity arises with the onset of reproduction (subadults not being modular) and is differentially expressed in males and females from different habitats. Both adult males and females show modularity in primordial, closed habitats. Overall, all these findings are important as they provide support to the idea that modularity can evolve at the population level and change fast within a species.

Sexual dimorphism in size and shape of traits related to locomotion in nine anuran species from Serbia and Montenegro

Investigation of sexual dimorphism patterns give us insight in how organisms adapt to fulfill their roles (reproductive, ecological, social) and enhance fitness. We examined sexual size and shape dimorphism in traits related to locomotion of nine anuran species from Serbia and Montenegro (Hyla arborea, Bombina variegata, Bufotes viridis, Rana temporaria, R. graeca, R. dalmatina, Pelophylax kl. esculentus, Pelobates fuscus and P. syriacus). Sexual size dimorphism in studied species ranges from female and male-biased, to absence of dimorphism. Sexual shape dimorphism was most pronounced in the forelimbs while the differences were small or did not exist in the hindlimbs and sacral traits. Males of most species were characterized by longer proximal parts (humerus and radioulna) and shorter distal forelimb parts, while the opposite pattern was observed in females. Also, some cases of significant intersexual shape differences are size-dependent. This indicates that these male traits are under stronger selective pressures to increase relative to body size, which may allow them to outcompete other males. Different types of behaviour can indirectly shape the limb morphology and lead to differences between the sexes. More data on the ecology and natural history of these animals are needed to explore the factors underlying the observed sex differences.

Morphometric ratio analyses: Locomotor mode in anurans

Current studies of anuran morphology use sacral vertebrae, hindlimbs as main predictor for locomotor modes, while forelimbs and their segments were not analysed in this context. Due the fact that the complex interplay of numerous morphological traits determines the locomotion ability of anurans, we used ratios for both fore- and hindlimbs to obtain useful information of the structural and functional properties of locomotor system. We examined patterns of variation in total length of fore-, and hindlimbs as well as sacral vertebrae width and diapophyseal expansion in order to position two locomotor modes (jumpers and walkers) in a morphological shape space. Further, we investigated patterns of variability in limbs proximal, medial and distal elements to highlight differences in intra- and inter-limb relations in two locomotor modes. Our results showed that the ratios between total hindlimb length and sacral width/diapophyseal expansion, as well as ratio between humerus and tibiofibula relate the most to locomotor modes. This implies that functional specialization in different locomotor modes is attained through modifications of ratios, not only within hindlimbs, but also through modifications of the whole integrated system, which consists of forelimb, hindlimb, and girdle elements.