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Active species reintroduction is an important conservation tool when aiming for the restoration of biological communities and ecosystems. The effective monitoring of reintroduction success is a crucial factor in this process. Here, we used a combination of environmental DNA (eDNA) techniques and species distribution models (SDMs) to evaluate the success of recent reintroductions of the freshwater fish Alburnoides bipunctatus in central Germany. We built SDMs without and with eDNA presence data to locate further suitable reintroduction sites and potentially overlooked populations of the species. We successfully detected eDNA of A. bipunctatus at all reintroduction sites, as well as several adjacent sites mostly in downstream direction, which supports the success of reintroduction efforts. eDNA‐based species detection considerably improved SDMs for A. bipunctatus, which allowed to identify species presence in previously unknown localities. Our results confirm the usefulness of eDNA techniques as standard tool to monitor reintroduced fish populations. We propose that combining eDNA with SDMs is a highly effective approach for long‐term monitoring of reintroduction success in aquatic species.
Background One of the central issues in ecology is the question what allows sympatric occurrence of closely related species in the same general area? The non-biting midges Chironomus riparius and C. piger, interbreeding in the laboratory, have been shown to coexist frequently despite of their close relatedness, similar ecology and high morphological similarity. Methodology/Principal Findings In order to investigate factors shaping niche partitioning of these cryptic sister species, we explored the actual degree of reproductive isolation in the field. Congruent results from nuclear microsatellite and mitochondrial haplotype analyses indicated complete absence of interspecific gene-flow. Autocorrelation analysis showed a non-random spatial distribution of the two species. Though not dispersal limited at the scale of the study area, the sister species occurred less often than expected at the same site, indicating past or present competition. Correlation and multiple regression analyses suggested the repartition of the available habitat along water chemistry gradients (nitrite, conductivity, CaCO3), ultimately governed by differences in summer precipitation regime. Conclusions We show that these morphologically cryptic sister species partition their niches due to a certain degree of ecological distinctness and total reproductive isolation in the field. The coexistence of these species provides a suitable model system for the investigation of factors shaping the distribution of closely related, cryptic species.
Although it has been suggested that temperature increase may alter the toxic potential of environmental pollutants, few studies have investigated the potential risk of chemical stressors for wildlife under Global Climate Change (GCC) impact. We applied a bifactorial multigeneration study in order to test if GCC conditions alter the effects of low pesticide concentrations on life history and genetic diversity of the aquatic model organism Chironomus riparius. Experimental populations of the species were chronically exposed to a low concentration of the fungicide pyrimethanil (half of the no-observed-adverse-effect concentration: NOAEC/2) under two dynamic present-day temperature simulations (11.0–22.7°C; 14.0–25.2°C) and one future scenario (16.5–28.1°C). During the 140-day multigeneration study, survival, emergence, reproduction, population growth, and genetic diversity of C. riparius were analyzed. Our results reveal that high temperature and pyrimethanil act synergistically on the midge C. riparius. In simulated present-day scenarios, a NOAEC/2 of pyrimethanil as derived from a life-cycle toxicity test provoked only slight-to-moderate beneficial or adverse effects on C. riparius. In contrast, exposure to a NOAEC/2 concentration of pyrimethanil at a thermal situation likely for a summer under GCC conditions uncovered adverse effects on mortality and population growth rate. In addition, genetic diversity was considerably reduced by pyrimethanil in the future scenario, but only slightly under current climatic conditions. Our multigeneration study under near-natural (climatic) conditions indicates that not only the impact of climate change, but also low concentrations of pesticides may pose a reasonable risk for aquatic insects in future.
The comeback of the Eurasian beaver (Castor fiber) throughout western and central Europe is considered a major conservation success. Traditionally, several subspecies are recognised by morphology and mitochondrial haplotype, each linked to a relict population. During various reintroduction programs in the 20th century, beavers from multiple source localities were released and now form viable populations. These programs differed in their reintroduction strategies, i.e., using pure subspecies vs. mixed source populations. This inhomogeneity in management actions generated ongoing debates regarding the origin of present beaver populations and appropriate management plans for the future. By sequencing of the mitochondrial control region and microsatellite genotyping of 235 beaver individuals from five selected regions in Germany, Switzerland, Luxembourg, and Belgium we show that beavers from at least four source origins currently form admixed, genetically diverse populations that spread across the study region. While regional occurrences of invasive North American beavers (n = 20) were found, all but one C. fiber bore the mitochondrial haplotype of the autochthonous western Evolutionary Significant Unit (ESU). Considering this, as well as the viability of admixed populations and the fact that the fusion of different lineages is already progressing in all studied regions, we argue that admixture between different beaver source populations should be generally accepted.
A range-wide synthesis and timeline for phylogeographic events in the red fox (Vulpes vulpes)
(2013)
Background: Many boreo-temperate mammals have a Pleistocene fossil record throughout Eurasia and North America, but only few have a contemporary distribution that spans this large area. Examples of Holarctic-distributed carnivores are the brown bear, grey wolf, and red fox, all three ecological generalists with large dispersal capacity and a high adaptive flexibility. While the two former have been examined extensively across their ranges, no phylogeographic study of the red fox has been conducted across its entire Holarctic range. Moreover, no study included samples from central Asia, leaving a large sampling gap in the middle of the Eurasian landmass.
Results: Here we provide the first mitochondrial DNA sequence data of red foxes from central Asia (Siberia), and new sequences from several European populations. In a range-wide synthesis of 729 red fox mitochondrial control region sequences, including 677 previously published and 52 newly obtained sequences, this manuscript describes the pattern and timing of major phylogeographic events in red foxes, using a Bayesian coalescence approach with multiple fossil tip and root calibration points. In a 335 bp alignment we found in total 175 unique haplotypes. All newly sequenced individuals belonged to the previously described Holarctic lineage. Our analyses confirmed the presence of three Nearctic- and two Japan-restricted lineages that were formed since the Mid/Late Pleistocene.
Conclusions: The phylogeographic history of red foxes is highly similar to that previously described for grey wolves and brown bears, indicating that climatic fluctuations and habitat changes since the Pleistocene had similar effects on these highly mobile generalist species. All three species originally diversified in Eurasia and later colonized North America and Japan. North American lineages persisted through the last glacial maximum south of the ice sheets, meeting more recent colonizers from Beringia during postglacial expansion into the northern Nearctic. Both brown bears and red foxes colonized Japan’s northern island Hokkaido at least three times, all lineages being most closely related to different mainland lineages. Red foxes, grey wolves, and brown bears thus represent an interesting case where species that occupy similar ecological niches also exhibit similar phylogeographic histories.
Large-scale genetic census of an elusive carnivore, the European wildcat (Felis s. silvestris)
(2016)
The European wildcat, Felis silvestris silvestris, serves as a prominent target species for the reconnection of central European forest habitats. Monitoring of this species, however, appears difficult due to its elusive behaviour and the ease of confusion with domestic cats. Recently, evidence for multiple wildcat occurrences outside its known distribution has accumulated in several areas across Central Europe, questioning the validity of available distribution data for this species. Our aim was to assess the fine-scale distribution and genetic status of the wildcat in its central European distribution range. We compiled and analysed genetic samples from roadkills and hundreds of recent hair-trapping surveys and applied phylogenetic and genetic clustering methods to discriminate wild and domestic cats and identify population subdivision. 2220 individuals were confirmed as either wildcat (n = 1792) or domestic cat (n = 342), and the remaining 86 (3.9 %) were identified as hybrids between the two. Remarkably, genetic distinction of domestic cats, wildcats and their hybrids was only possible when taking into account the presence of two highly distinct genetic lineages of wildcats, with a suture zone in central Germany. 44 % of the individual wildcats where sampled outside the previously published distribution. Our analyses confirm a relatively continuous spatial presence of wildcats across large parts of the study area in contrast to previous analyses indicating a highly fragmented distribution. Our results suggest that wildcat conservation and management should take advantage of the higher than previously assumed dispersal potential of wildcats, which may use wildlife corridors very efficiently.
Background: Understanding the processes that lead to hybridization of wolves and dogs is of scientific and management importance, particularly over large geographical scales, as wolves can disperse great distances. However, a method to efficiently detect hybrids in routine wolf monitoring is lacking. Microsatellites offer only limited resolution due to the low number of markers showing distinctive allele frequencies between wolves and dogs. Moreover, calibration across laboratories is time-consuming and costly. In this study, we selected a panel of 96 ancestry informative markers for wolves and dogs, derived from the Illumina CanineHD Whole-Genome BeadChip (174 K). We designed very short amplicons for genotyping on a microfluidic array, thus making the method suitable also for non-invasively collected samples.
Results: Genotypes based on 93 SNPs from wolves sampled throughout Europe, purebred and non-pedigree dogs, and suspected hybrids showed that the new panel accurately identifies parental individuals, first-generation hybrids and first-generation backcrosses to wolves, while second- and third-generation backcrosses to wolves were identified as advanced hybrids in almost all cases. Our results support the hybrid identity of suspect individuals and the non-hybrid status of individuals regarded as wolves. We also show the adequacy of these markers to assess hybridization at a European-wide scale and the importance of including samples from reference populations.
Conclusions: We showed that the proposed SNP panel is an efficient tool for detecting hybrids up to the third-generation backcrosses to wolves across Europe. Notably, the proposed genotyping method is suitable for a variety of samples, including non-invasive and museum samples, making this panel useful for wolf-dog hybrid assessments and wolf monitoring at both continental and different temporal scales.
Wolves (Canis lupus) are currently showing a remarkable comeback in the highly frag-mented cultural landscapes of Germany. We here show that wolf numbers increasedexponentially between 2000 and 2015 with an annual increase of about 36%. Wedemonstrate that the first territories in each newly colonized region were establishedover long distances from the nearest known reproducing pack on active militarytraining areas (MTAs). We show that MTAs, rather than protected areas, served asstepping-stones for the recolonization of Germany facilitating subsequent spreadingof wolf territories in the surrounding landscape. We did not find any significant differ-ence between MTAs and protected areas with regard to habitat. One possible reasonfor the importance of MTAs may be their lower anthropogenic mortality rates com-pared to protected and other areas. To our knowledge, this is the first documented casewhere MTAs facilitate the recolonization of an endangered species across large areas.
Freshwater biodiversity has declined dramatically in Europe in recent decades. Because of massive habitat pollution and morphological degradation of water bodies, many once widespread species persist in small fractions of their original range. These range contractions are generally believed to be accompanied by loss of intraspecific genetic diversity, due to the reduction of effective population sizes and the extinction of regional genetic lineages. We aimed to assess the loss of genetic diversity and its significance for future potential reintroduction of the long-tailed mayfly Palingenia longicauda (Olivier), which experienced approximately 98% range loss during the past century. Analysis of 936 bp of mitochondrial DNA of 245 extant specimens across the current range revealed a surprisingly large number of haplotypes (87), and a high level of haplotype diversity (Hd = 0.875). In contrast, historic specimens (6) from the lost range (Rhine catchment) were not differentiated from the extant Rába population (F ST = 0.02, p = 0.61), despite considerable geographic distance separating the two rivers. These observations can be explained by an overlap of the current with the historic (Pleistocene) refugia of the species. Most likely, the massive recent range loss mainly affected the range which was occupied by rapid post-glacial dispersal. We conclude that massive range losses do not necessarily coincide with genetic impoverishment and that a species' history must be considered when estimating loss of genetic diversity. The assessment of spatial genetic structures and prior phylogeographic information seems essential to conserve once widespread species.
The recent recolonisation of the Central European lowland (CEL) by the grey wolf (Canis lupus) provides an excellent opportunity to study the effect of founder events on endoparasite diversity. Which role do prey and predator populations play in the re-establishment of endoparasite life cycles? Which intrinsic and extrinsic factors control individual endoparasite diversity in an expanding host population? In 53 individually known CEL wolves sampled in Germany, we revealed a community of four cestode, eight nematode, one trematode and 12 potential Sarcocystis species through molecular genetic techniques. Infections with zoonotic Echinococcus multilocularis, Trichinella britovi and T. spiralis occurred as single cases. Per capita endoparasite species richness and diversity significantly increased with population size and changed with age, whereas sex, microsatellite heterozygosity, and geographic origin had no effect. Tapeworm abundance (Taenia spp.) was significantly higher in immigrants than natives. Metacestode prevalence was slightly higher in ungulates from wolf territories than from control areas elsewhere. Even though alternative canid definitive hosts might also play a role within the investigated parasite life cycles, our findings indicate that (1) immigrated wolves increase parasite diversity in German packs, and (2) prevalence of wolf-associated parasites had declined during wolf absence and has now risen during recolonisation.
Following severe population decline and local extinction due to massive habitat destruction and persecution, wildcats have recently reappeared in several parts of Germany’s low mountain region. It remains unknown how this reemergence occurred, specifically if local populations have been overlooked at low densities or if the species has successfully spread across the highly fragmented anthropogenic landscape. In the central German Rhön Mountains, for instance, wildcats were believed to be extinct during most of the twentieth century, however, the species was recently detected and subsequent genetic monitoring found the presence of a sizeable population. In this study, we used microsatellite and SNP genotypes from 146 wildcat individuals from 2008 to 2017 across a ~ 15,000 km2 area in the central German low mountain region to understand the population re-establishment of wildcats in the region. Bayesian clustering and subsequent analyses revealed that animals in the Rhön Mountains appear to be a mix from the two adjacent populations in the North and South of the area, suggesting a recent range expansion from two different directions. Both populations meet in the Rhön Biosphere Reserve, leading to an admixture of the northern, autochthonous, and the southern reintroduced wildcat population. While we cannot completely exclude the possibility of undetected population persistence, the high genetic homogeneity in the central German wildcat population and the lack of any signatures of past population decline in the Rhön favor a scenario of natural expansion. Our findings thus suggest that wildcats are well capable of rapid range expansion across richly structured landscape mosaics consisting of open land, settlements, and forest patches and document the potential of massive non-invasive genetic sampling when aiming to reconstruct the complex population and range dynamics of wildlife.
The rate of species extinctions due to anthropogenic activities has dramatically increased within the past few centuries (Dirzo & Raven, 2003; Novacek & Cleland, 2001). Although the mechanisms and ultimate causes leading to the extinction of species remain largely unclear (Frankham et al., 2002), five threats to global biodiversity have frequently been referred to as the most important: habitat destruction and fragmentation, global climate change, hunting and overuse of food resources, biological invasions and environmental pollution (Dudgeon et al., 2006; Lewis, 2006; Novacek & Cleland, 2001). Different research fields, as conservation biology, ecology and ecotoxicology, investigate the effects of these factors on organisms and found strong evidence for their negative impact on regional and global biodiversity.
In most cases, natural populations will be impacted not only by one threat, but rather a combination of them (Buckley & Roughgarden, 2004; Kappelle et al., 1999). Multiple environmental stress factors can have cumulative negative effects on the survival of populations (Sih et al., 2004). To understand, how natural populations respond to combinations of different stress factors is thus of crucial importance in order to understand our present and future impact on all scales of biodiversity (Warren et al., 2001).
The effects of anthropogenically introduced chemicals on organisms and ecosystems are investigated in the field of ecotoxicology. Research in this area has led to a large body of information concerning the impact of chemical stress on the fitness of model species in the laboratory. In contrast to this, there is an obvious lack of knowledge on the effects of contaminants on natural populations and communities (Bickham et al., 2000; Bourdeau et al., 1990). For instance, ecotoxicologists have just started to investigate the impact of environmental pollution on the genetic variability of natural populations (Bickham et al., 2000; Whitehead et al., 2003). Genetic variation provides the raw material for populations in order to adapt to changing environmental conditions and is thus the substrate for evolution and long-term survival of populations and species (Frankham, 2005). The amount of genetic variation in populations is positively correlated with the effective population size (Frankham, 1996). Habitat destruction and fragmentation has divided the ranges of many species into small and isolated refuges. Without migration from adjacent habitats, isolated populations will decrease in their level of genetic diversity through random loss of alleles (Hedrick, 2000). Frankham (1995) for instance, showed that 32 of the 37 endangered species (which occur in small populations per definition) of different animals and plant taxa display reduced levels of heterozygosity compared to closely related and more frequent species.
In strongly human impacted landscapes, both factors, environmental pollution and habitat destruction, can be expected to occur frequently together. It is thus of crucial importance to investigate the impact of reduced genetic diversity and inbreeding on the response to chemical stress. In addition, chemical exposure has frequently been discussed to have an impact on the extent of genetic variability in exposed populations (Guttman, 1994; Staton et al., 2001; van Straalen & Timmermans, 2002). However, evidence for this 'genetic erosion hypothesis' remained scarce to date, most likely because of the difficulty to single out the impact of pollution stress from a background of multiple factors which influence patterns of genetic variability in natural populations (Belfiore, 2001; Staton et al., 2001; van Straalen & Timmermans, 2002).
The European bison was saved from the brink of extinction due to considerable conservation efforts since the early 20th century. The current global population of > 9,500 individuals is the result of successful ex situ breeding based on a stock of only 12 founders, resulting in an extremely low level of genetic variability. Due to the low allelic diversity, traditional molecular tools, such as microsatellites, fail to provide sufficient resolution for accurate genetic assessments in European bison, let alone from non-invasive samples. Here, we present a SNP panel for accurate high-resolution genotyping of European bison, which is suitable for a wide variety of sample types. The panel accommodates 96 markers allowing for individual and parental assignment, sex determination, breeding line discrimination, and cross-species detection. Two applications were shown to be utilisable in further Bos species with potential conservation significance. The new SNP panel will allow to tackle crucial tasks in European bison conservation, including the genetic monitoring of reintroduced populations, and a molecular assessment of pedigree data documented in the world’s first studbook of a threatened species.