Cryptic phylogeographic diversifications provide unique models to examine the role of phylogenetic divergence on the evolution of reproductive isolation, without extrinsic factors such as ecological and behavioural differentiation. Yet, to date very few comparative studies have been attempted within such radiations. Here, we characterize a new speciation continuum in a group of widespread Eurasian amphibians, the Pelobates spadefoot toads, by conducting multilocus (restriction site associated DNA sequencing and mitochondrial DNA) phylogenetic, phylogeographic and hybrid zone analyses. Within the P. syriacus complex, we discovered species‐level cryptic divergences (>5 million years ago [My]) between populations distributed in the Near‐East (hereafter P. syriacus sensu stricto [s.s.]) and southeastern Europe (hereafter P. balcanicus), each featuring deep intraspecific lineages. Altogether, we could scale hybridizability to divergence time along six different stages, spanning from sympatry without gene flow (P. fuscus and P. balcanicus, >10 My), parapatry with highly restricted hybridization (P. balcanicus and P. syriacus s.s., >5 My), narrow hybrid zones (~15 km) consistent with partial reproductive isolation (P. fuscus and P. vespertinus, ~3 My), to extensive admixture between Pleistocene and refugial lineages (≤2 My). This full spectrum empirically supports a gradual build up of reproductive barriers through time, reversible up until a threshold that we estimate at ~3 My. Hence, cryptic phylogeographic lineages may fade away or become reproductively isolated species simply depending on the time they persist in allopatry, and without definite ecomorphological divergence.
Vipera ursinii graeca is a restricted-range, endemic snake of the Pindos mountain range in the southwestern Balkans. The subspecies was previously reported from eight localities in Greece and one locality in southern Albania. We used species distribution modelling based on climate data from known localities in Greece to estimate the potential distribution of the subspecies. The model predicted suitable areas for eleven mountains in southern Albania, which we visited in ten field expeditions in four years. Based on 78 live individuals and 33 shed skins, we validated the presence of the snake on eight of the eleven mountains. Six populations (Dhëmbel, Llofiz, Griba, Shendelli, Tomorr and Trebeshinë Mountains) are reported here for the first time. Morphological characters undoubtedly supported that all individuals found at these new localities belong to V. u. graeca. Genetic analysis of mitochondrial DNA sequences also confirmed the identity of the snakes as V. u. graeca and a low number of identified haplotypes suggested low genetic variability among populations despite significant spatial isolation. All localities were subalpine-alpine calcareous meadows above 1600 m. These high montane habitats are separated by deep valleys and are threatened by overgrazing, soil erosion, and a potential increase in the elevation of the tree line due to climate change. Our surveys increased the number of known populations by 60% and the known geographical range of the subspecies by approximately 30%. Our study serves as a baseline for further ecological research and for conservation measures for one of the least known European viperid snakes.
Meadow vipers (Vipera ursinii-renardi complex) are small-bodied snakes that live in either lowland grasslands or montane subalpine-alpine meadows spanning a distribution from France to western China. This complex has previously been the focus of several taxonomic studies which were based mainly on morphological, allozyme or immunological characters and did not clearly resolve the relationships between the various taxa. Recent mitochondrial DNA analyses found unexpected relationships within the complex which had taxonomical consequences for the detected lineages. The most surprising was the basal phylogenetic position of Vipera ursinii graeca, a taxon described almost 30 years ago from the mountains of Greece. We present here new analyses of three nuclear markers (BDNF, NT3, PRLR; a first for studies of meadow and steppe vipers) as well as analyses of newly obtained mitochondrial DNA sequences (CYT B, ND4).Our Bayesian analyses of nuclear sequences are concordant with previous studies of mitochondrial DNA, in that the phylogenetic position of the graeca clade is a clearly distinguished and distinct lineage separated from all other taxa in the complex. These phylogenetic results are also supported by a distinct morphology, ecology and isolated distribution of this unique taxon. Based on several data sets and an integrative species concept we recommend to elevate this taxon to species level: Vipera graeca Nilson & Andrén, 1988 stat. nov.
Grassland ecosystems are among the most threatened biomes, and their restoration has become common in nature conservation. Yet restoration is rarely applied specifically for reptiles, which are among the most threatened vertebrates. The Meadow Viper (Vipera ursinii) has become extinct in most of lowland Europe, and an endangered subspecies (Vipera ursinii rakosiensis) has been a target of habitat restoration and captive breeding in Hungary since 2004. We quantified vegetation properties and the density of reptiles that either spontaneously colonised (three species) or were reintroduced (V. ursinii) in a grassland restored specifically for this purpose. We used a fine-scale survey to estimate the cover, and compositional and vertical diversity of the vegetation. We characterised sampling units along three habitat gradients: wetness, openness and grass tussock size. Model selection based on data from replicated counts showed that Green Lizards (Lacerta viridis) responded positively to vegetation cover and negatively to tussock area and height, and number of burrows. The Sand Lizard (Lacerta agilis) responded positively to vegetation cover, vertical diversity and wetness, and negatively to openness. The Balkan Wall Lizard (Podarcis tauricus) responded positively to tussock height and negatively to vegetation cover. Finally, V. ursinii responded positively to vegetation cover and tussock height, and negatively to compositional diversity. Our results show the general importance of structural and compositional diversity of vegetation to reptiles. These results suggest that adaptive management should focus on increasing the total cover (for lizards) and the structural diversity of vegetation (for each species) to benefit reptiles in restored grasslands.
Spatial prioritization in systematic conservation planning has traditionally been developed for several to many species and/or habitats, and single-species applications are rare. We developed a novel spatial prioritization model based on accurate estimates of remotely-sensed data and maps of threats potentially affecting long-term species persistence. We used this approach to identify priority areas for the conservation of the Endangered Greek meadow viper Vipera graeca, a cold-adapted species inhabiting mountaintops in the Pindos Mountains of Greece and Albania. We transformed the mapped threats into nine variables to estimate conservation value: habitat suitability (climate suitability, habitat size, occupancy, vegetation suitability), climate change (future persistence, potential for altitudinal range shift) and land-use impact (habitat alteration, degradation, disturbance). We applied the Zonation systematic conservation planning tool with these conservation value variables as biodiversity features to rank the areas currently occupied by the species and to identify priority areas where the chances for population persistence are highest. We found that 90% of current habitats will become unsuitable by the 2080s and that conservation actions need to be implemented to avoid extinction as this is already a threatened species with a narrow ecological niche. If threats are appropriately quantified and translated into variables of conservation value, spatial conservation planning tools can successfully identify priority areas for the conservation of single species. Our study demonstrates that spatial prioritization for single umbrella, flagship or keystone species is a promising approach for the conservation of species for which few data are available.
Ecosystem restoration implies focusing on multiple trophic levels and ecosystem functioning, yet higher trophic levels, that is, animals, are less frequently targeted by restoration than plants. Habitat diversity, the spatial heterogeneity between and within habitat patches in a landscape, is a well-known driver of species diversity, and offers possible ways to increase species diversity at multiple trophic levels. We argue that habitat diversity is central in whole-ecosystem restoration as we review its importance, provide a practical definition for its components, and propose ways to target it in restoration. Restoration targeting habitat diversity is used commonly in aquatic ecosystems, mostly to increase the physical diversity of habitats, meant to provide more niches available to a higher number of animal species. To facilitate the uptake of habitat diversity in terrestrial ecosystem restoration, we distinguish between compositional and structural habitat diversity, because different animal groups will respond to different aspects of habitat diversity. We also propose four methods to increase habitat diversity: varying the starting conditions to obtain divergent successional pathways, emulating natural disturbances, establishing keystone structures, and applying ecosystem engineer species. We provide two case studies to illustrate how these components and methods can be incorporated in restoration. We conclude that targeting habitat diversity is a promising way to restore habitats for a multitude of species of animals and plants, and that it should become mainstream in restoration ecology and practice. We encourage the restoration community to consider compositional and structural habitat diversity and to specifically target habitat diversity in ecosystem restoration.
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