Development of SNP markers identifying European wildcats,domestic cats,and their admixed progeny

Introgression can be an important evolutionary force but it can also lead to species extinction and as such is a crucial issue for species conservation. However, introgression is difficult to detect, morphologically as well as genetically. Hybridization with domestic cats (Felis silvestris catus) is a major concern for the conservation of European wildcats (Felis s. silvestris). The available morphologic and genetic markers for the two Felis subspecies are not sufficient to reliably detect hybrids beyond first generation. Here we present a single nucleotide polymorphism (SNP) based approach that allows the identification of introgressed individuals. Using high‐throughput sequencing of reduced representation libraries we developed a diagnostic marker set containing 48 SNPs (Fst  > 0.8) which allows the identification of wildcats, domestic cats, their hybrids and backcrosses. This allows assessing introgression rate in natural wildcat populations and is key for a better understanding of hybridization processes.     

How reliable are morphological and anatomical characters to distinguish European wildcats,domestic cats and their hybrids in France?

Phenotypic variation in hybridizing species or subspecies is a prerequisite for allowing conservation ecologists and wildlife managers to identify parental populations and their hybrids in the field. We assessed the reliability of a set of eight morphological (body size and pelage characters) and four anatomical criteria (skull and intestine morphometric measurements) to distinguish between 302 French specimens classified as wildcat, domestic cat or hybrid on the basis of a Bayesian analysis (STRUCTURE) of their multilocus microsatellite genotypes. This aim was achieved by performing a set of multivariate analyses on morphological, anatomical and genetic data sets (Hill and Smith's analysis, co‐inertia analysis and discriminant analysis of principal components). Wildcats and domestic cats were very satisfactorily distinguished, even when using simple non‐invasive morphological criteria easily usable in the field like the morphology of the tail, dorsal line or flank stripes. Using anatomical instead of morphological characters slightly increased the discriminating power. Many more difficulties arose when we tried to distinguish hybrid specimens from both wildcat and domestic ones. Anatomical characters performed better than morphological ones in recognizing hybrids, but the assignment success rate remained very low, about 31.6% and 1.5%, respectively. Overall, the most discriminating characters were two continuous, derived anatomical characters: the cranial index followed by the intestinal index. Classification of specimens in three classes based on their microsatellite genotypes appeared to be inadequate for identifying hybrid specimens, as hybrid specimens seemed to be distributed along an anatomical continuum. With this observation in mind, we assessed the linear relationships between a proxy of the individual level of hybridization (q_ik) and the cranial and intestinal indices, respectively. Both relationships were highly significant. The greatest correlation was found with the cranial index (R² = 60.4%). Altogether, our results suggest that future work should be geared towards enhancing the measure of hybridization using more discriminating molecular markers and improving morphometric skull measurements through the use of modern geometric morphometric methods, using landmarks rather than skull dimension.     

Gene flow and population structure of a solitary top carnivore in a human‐dominated landscape

While African leopard populations are considered to be continuous as demonstrated by their high genetic variation, the southernmost leopard population exists in the Eastern and Western Cape, South Africa, where anthropogenic activities may be affecting this population's structure. Little is known about the elusive, last free‐roaming top predator in the region and this study is the first to report on leopard population structuring using nuclear DNA. By analyzing 14 microsatellite markers from 40 leopard tissue samples, we aimed to understand the populations' structure, genetic distance, and gene flow (Nm). Our results, based on spatially explicit analysis with Bayesian methods, indicate that leopards in the region exist in a fragmented population structure with lower than expected genetic diversity. Three population groups were identified, between which low to moderate levels of gene flow were observed (Nm 0.5 to 3.6). One subpopulation exhibited low genetic differentiation, suggesting a continuous population structure, while the remaining two appear to be less connected, with low emigration and immigration between these populations. Therefore, genetic barriers are present between the subpopulations, and while leopards in the study region may function as a metapopulation, anthropogenic activities threaten to decrease habitat and movement further. Our results indicate that the leopard population may become isolated within a few generations and suggest that management actions should aim to increase habitat connectivity and reduce human–carnivore conflict. Understanding genetic diversity and connectivity of populations has important conservation implications that can highlight management of priority populations to reverse the effects of human‐caused extinctions.     

Population genetic patterns among social groups of the endangered Central American spider monkey (Ateles geoffroyi) in a human‐dominated landscape

Spider monkeys (Genus: Ateles) are a widespread Neotropical primate with a highly plastic socioecological strategy. However, the Central American species, Ateles geoffroyi, was recently re‐listed as endangered due to the accelerated loss of forest across the subcontinent. There is inconsistent evidence that spider monkey populations could persist when actively protected, but their long‐term viability in unprotected, human‐dominated landscapes is not known. We analyzed noninvasive genetic samples from 185 individuals in 14 putative social groups on the Rivas Isthmus in southwestern Nicaragua. We found evidence of weak but significant genetic structure in the mitochondrial control region and in eight nuclear microsatellite loci plus negative spatial autocorrelation in Fst and kinship. The overall pattern suggests strong localized mating and at least historical female‐biased dispersal, as is expected for this species. Heterozygosity was significantly lower than expected under random mating and lower than that found in other spider monkey populations, possibly reflecting a recent decline in genetic diversity and a threat from inbreeding. We conclude that despite a long history of human disturbance on this landscape, spider monkeys were until recently successful at maintaining gene flow. We consider the recent decline to be further indication of accelerated anthropogenic disturbance, but also of an opportunity to conserve native biodiversity. Spider monkeys are one of many wildlife species in Central America that is threatened by land cover change, and an apt example of how landscape‐scale conservation planning could be used to ensure long‐term persistence.     

Canid hybridization: contemporary evolution in human‐modified landscapes

Contemporary evolution through human‐induced hybridization occurs throughout the taxonomic range. Formerly allopatric species appear especially susceptible to hybridization. Consequently, hybridization is expected to be more common in regions with recent sympatry owing to human activity than in areas of historical range overlap. Coyotes ( Canis latrans) and gray wolves ( C. lupus) are historically sympatric in western North America. Following European settlement gray wolf range contracted, whereas coyote range expanded to include eastern North America. Furthermore, wolves with New World (NW) mitochondrial DNA (mtDNA) haplotypes now extend from Manitoba to Québec in Canada and hybridize with gray wolves and coyotes. Using mtDNA and 12 microsatellite markers, we evaluated levels of wolf‐coyote hybridization in regions where coyotes were present (the Canadian Prairies, n = 109 samples) and absent historically (Québec, n = 154). Wolves with NW mtDNA extended from central Saskatchewan (51°N, 69°W) to northeastern Québec (54°N, 108°W). On the Prairies, 6.3% of coyotes and 9.2% of wolves had genetic profiles suggesting wolf‐coyote hybridization. In contrast, 12.6% of coyotes and 37.4% of wolves in Québec had profiles indicating hybrid origin. Wolves with NW and Old World ( C. lupus) mtDNA appear to form integrated populations in both regions. Our results suggest that hybridization is more frequent in historically allopatric populations. Range shifts, now expected across taxa following climate change and other human influence on the environment, might therefore promote contemporary evolution by hybridization.     

Hybridization between Felis silvestris silvestris and Felis silvestris catus in two contrasted environments in France

European wildcat (Felis silvestris silvestris) populations are fragmented throughout most of the whole range of the subspecies and may be threatened by hybridization with the domestic cat F.s. catus. The underlying ecological processes promoting hybridization remain largely unknown. In France, wildcats are mainly present in the northeast and signs of their presence in the Pyrenees have been recently provided. However, no studies have been carried out in the French Pyrenees to assess their exposure to hybridization. We compared two local populations of wildcats, one living in a continuous forest habitat in the French Pyrenees, the other living in a highly fragmented forest‐agricultural landscape in northeastern France to get insights into the variability of hybridization rates. Strong evidence of hybridization was detected in northeastern France and not in the Pyrenees. Close kin in the Pyrenees were not found in the same geographic location contrary to what was previously reported for females in the northeastern wildcat population. The two wildcat populations were significantly differentiated (F_ST = 0.072) to an extent close to what has been reported (F_ST = 0.103) between the Iberian population, from which the Pyrenean population may originate, and the German population, which is connected to the northeastern population. The genetic diversity of the Pyrenean wildcats was lower than that of northeastern wildcat populations in France and in other parts of Europe. The lower hybridization in the Pyrenees may result from the continuity of natural forest habitats. Further investigations should focus on linking landscape features to hybridization rates working on local populations.     

Variation of cats under domestication: genetic assignment of domestic cats to breeds and worldwide random‐bred populations

Both cat breeders and the lay public have interests in the origins of their pets, not only in the genetic identity of the purebred individuals, but also in the historical origins of common household cats. The cat fancy is a relatively new institution with over 85% of its 40–50 breeds arising only in the past 75 years, primarily through selection on single‐gene aesthetic traits. The short, yet intense cat breed history poses a significant challenge to the development of a genetic marker–based breed identification strategy. Using different breed assignment strategies and methods, 477 cats representing 29 fancy breeds were analysed with 38 short tandem repeats, 148 intergenic and five phenotypic single nucleotide polymorphisms. Results suggest the frequentist method of Paetkau (single nucleotide polymorphisms = 0.78, short tandem repeats = 0.88) surpasses the Bayesian method of Rannala and Mountain (single nucleotide polymorphisms = 0.56, short tandem repeats = 0.83) for accurate assignment of individuals to the correct breed. Additionally, a post‐assignment verification step with the five phenotypic single nucleotide polymorphisms accurately identified between 0.31 and 0.58 of the misassigned individuals raising the sensitivity of assignment with the frequentist method to 0.89 and 0.92 for single nucleotide polymorphisms and short tandem repeats respectively. This study provides a novel multistep assignment strategy and suggests that, despite their short breed history and breed family groupings, a majority of cats can be assigned to their proper breed or population of origin, that is, race.     

Contemporary human‐altered landscapes and oceanic barriers reduce bumble bee gene flow

Much of the world's terrestrial landscapes are being altered by humans in the form of agriculture, urbanization and pastoral systems, with major implications for biodiversity. Bumble bees are one of the most effective pollinators in both natural and cultivated landscapes, but are often the first to be extirpated in human‐altered habitats. Yet, little is known about the role of natural and human‐altered habitats in promoting or limiting bumble bee gene flow. In this study, I closely examine the genetic structure of the yellow‐faced bumble bee, Bombus vosnesenskii, across the southwestern US coast and find strong evidence that natural oceanic barriers, as well as contemporary human‐altered habitats, limit bee gene flow. Heterozygosity and allelic richness were lower in island populations, while private allelic richness was higher in island populations compared to mainland populations. Genetic differentiation, measured for three indices across the 1000 km study region, was significantly greater than the null expectation (F_ST = 0.041, F’_ST = 0.044 and D_est = 0.155) and correlated with geographic distance. Furthermore, genetic differentiation patterns were most strongly correlated with contemporary (2011) not past (2006, 2001) resistance maps calibrated for high dispersal limitation over oceans, impervious habitat and croplands. Despite the incorporation of dramatic elevation gradients, the analyses reveal that oceans and contemporary human land use, not mountains, are the primary dispersal barriers for B. vosnesenskii gene flow. These findings reinforce the importance of maintaining corridors of suitable habitat across the distribution range of native pollinators to promote their persistence and safeguard their ability to provide essential pollination services.     

Deep mitochondrial introgression and hybridization among ecologically divergent vole species

The completion of speciation is typically difficult to ascertain in rapidly diverging taxa but the amount of hybridization and gene flow in sympatry or parapatry contains important information about the level of reproductive isolation achieved. Here, we examined the progress in speciation between the Mediterranean (Microtus duodecimcostatus) and the Lusitanian pine vole (M. lusitanicus), which are part of the most rapid radiation of species known in mammals. These two Iberian pine voles are classified as separate species because of differences in morphology and ecology, but relatively many ambiguous individuals can be found in sympatric conditions. Our phylogenetic analyses of rangewide data from the mitochondrial cytochrome b gene (mtDNA) demonstrated high levels of diversity and a basal separation in two parapatric lineages. However, mtDNA affiliation was at odds with morphological classification or geographical distribution of the taxa. In contrast, statistical analyses of microsatellites (nucDNA) showed two clear genetic clusters in allopatry and sympatry generally matching morphological classification. This cytonuclear discordance over a large geographic area suggests historical introgression of mtDNA from M. duodecimcostatus to M. lusitanicus. There was statistical evidence for at least two recent hybrids in the sympatry zone but gene flow is apparently low given clear‐cut differences in nucDNA. Our results indicate a relatively advanced speciation process in these Iberian pine voles without fully established reproductive isolation. This situation enables use of combined population genomic and experimental approaches for the separation of patterns and mechanisms in the ongoing explosive diversification of these and other Arvicoline rodents in the future.     

Response of feral cats to a track‐based baiting programme using Eradicat® baits

The feral Cat (Felis catus) is a significant threat to Australian fauna, and reducing their impacts is considered an essential action for threatened species conservation. Poison baiting is increasingly being used for the broad scale control of feral cats. In this study, we measured the population response of feral cats to a track‐based baiting programme using Eradicat^® baits in the semi‐arid northern wheatbelt region of Western Australia. Over two years, 1500 baits were laid once annually and the response of feral cats was measured using remote cameras in a before–after, control–impact design. There was a significant reduction in feral cat activity in the second year, but not the first. During bait uptake trials, corvids removed the most number of baits, followed by cats and varanids. The lack of a response to baiting in the first year may be due to existing low cat numbers in the baited area and/or the timing of the baiting. We provide a list of key recommendations to help inform future cat baiting programmes and research.     

Strong spatial segregation between wildcats and domestic cats may explain low hybridization rates on the Iberian Peninsula

The European wildcat (Felis silvestris silvestris) is an endangered felid impacted by genetic introgression with the domestic cat (Felis silvestris catus). The problem of hybridization has had different effects in different areas. In non-Mediterranean regions pure forms of wildcats became almost extinct, while in Mediterranean regions genetic introgression is a rare phenomenon. The study of the potential factors that prevent the gene flow in areas of lower hybridization may be key to wildcat conservation. We studied the population size and spatial segregation of wildcats and domestic cats in a typical Mediterranean area of ancient sympatry, where no evidence of hybridization had been detected by genetic studies. Camera trapping of wild-living cats and walking surveys of stray cats in villages were used for capture–recapture estimations of abundance and spatial segregation. Results showed (i) a low density of wildcats and no apparent presence of putative hybrids; (ii) a very low abundance of feral cats in spite of the widespread and large population sources of domestic cats inhabiting villages; (iii) strong spatial segregation between wildcats and domestic/feral cats; and (iv) no relationship between the size of the potential population sources and the abundance of feral cats. Hence, domestic cats were limited in their ability to become integrated into the local habitat of wildcats. Ecological barriers (habitat preferences, food limitations, intra-specific and intra-guild competition, predation) may explain the severe divergences of hybridization impact observed at a biogeographic level. This has a direct effect on key conservation strategies for wildcats (i.e., control of domestic cats).     

Death by sex in an Australian icon: a continent‐wide survey reveals extensive hybridization between dingoes and domestic dogs

Hybridization between domesticated animals and their wild counterparts can disrupt adaptive gene combinations, reduce genetic diversity, extinguish wild populations and change ecosystem function. The dingo is a free‐ranging dog that is an iconic apex predator and distributed throughout most of mainland Australia. Dingoes readily hybridize with domestic dogs, and in many Australian jurisdictions, distinct management strategies are dictated by hybrid status. Yet, the magnitude and spatial extent of domestic dog–dingo hybridization is poorly characterized. To address this, we performed a continent‐wide analysis of hybridization throughout Australia based on 24 locus microsatellite DNA genotypes from 3637 free‐ranging dogs. Although 46% of all free‐ranging dogs were classified as pure dingoes, all regions exhibited some hybridization, and the magnitude varied substantially. The southeast of Australia was highly admixed, with 99% of animals being hybrids or feral domestic dogs, whereas only 13% of the animals from remote central Australia were hybrids. Almost all free‐ranging dogs had some dingo ancestry, indicating that domestic dogs could have poor survivorship in nonurban Australian environments. Overall, wild pure dingoes remain the dominant predator over most of Australia, but the speed and extent to which hybridization has occurred in the approximately 220 years since the first introduction of domestic dogs indicate that the process may soon threaten the persistence of pure dingoes.     

Refugia,colonization and diversification of an arid‐adapted bird: coincident patterns between genetic data and ecological niche modelling

Phylogeographical studies are common in boreal and temperate species from the Palaearctic, but scarce in arid‐adapted species. We used nuclear and mitochondrial markers to investigate phylogeography and to estimate chronology of colonization events of the trumpeter finch Bucanetes githagineus, an arid‐adapted bird. We used 271 samples from 16 populations, most of which were fresh samples but including some museum specimens. Microsatellite data showed no clear grouping according to the sampling locations. Microsatellite and mitochondrial data showed the clearest differentiation between Maghreb and Canary Islands and between Maghreb and Western Sahara. Mitochondrial data suggest differentiation between different Maghreb populations and among Maghreb and Near East populations, between Iberian Peninsula and Canary Islands, as well as between Western Sahara and Maghreb. Our coalescence analyses indicate that the trumpeter finch colonized North Africa during the humid Marine Isotope Stage 5 (MIS5) period of the Sahara region 125 000 years ago. We constructed an ecological niche model (ENM) to estimate the geographical distribution of climatically suitable habitats for the trumpeter finch. We tested whether changes in the species range in relation to glacial–interglacial cycles could be responsible for observed patterns of genetic diversity and structure. Modelling results matched with those from genetic data as the species' potential range increases in interglacial scenarios (in the present climatic scenario and during MIS5) and decreases in glacial climates (during the last glacial maximum, LGM, 21 000 years ago). Our results suggest that the trumpeter finch responded to Pleistocene climatic changes by expanding and contracting its range.     

Feral Cat Globetrotters: genetic traces of historical human‐mediated dispersal

Endemic species on islands are highly susceptible to local extinction, in particular if they are exposed to invasive species. Invasive predators, such as feral cats, have been introduced to islands around the world, causing major losses in local biodiversity. In order to control and manage invasive species successfully, information about source populations and level of gene flow is essential. Here, we investigate the origin of feral cats of Hawaiian and Australian islands to verify their European ancestry and a potential pattern of isolation by distance. We analyzed the genetic structure and diversity of feral cats from eleven islands as well as samples from Malaysia and Europe using mitochondrial DNA (ND5 and ND6 regions) and microsatellite DNA data. Our results suggest an overall European origin of Hawaiian cats with no pattern of isolation by distance between Australian, Malaysian, and Hawaiian populations. Instead, we found low levels of genetic differentiation between samples from Tasman Island, Lana'i, Kaho'olawe, Cocos (Keeling) Island, and Asia. As these populations are separated by up to 10,000 kilometers, we assume an extensive passive dispersal event along global maritime trade routes in the beginning of the 19th century, connecting Australian, Asian, and Hawaiian islands. Thus, islands populations, which are characterized by low levels of current gene flow, represent valuable sources of information on historical, human‐mediated global dispersal patterns of feral cats.     

Evolutionary and ecological traps for brown bears Ursus arctos in human‐modified landscapes

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Toucans (Ramphastos ambiguus) facilitate resilience against seed dispersal limitation to a large‐seeded tree (Virola surinamensis) in a human‐modified landscape

Large‐seeded plants may suffer seed dispersal limitation in human‐modified landscapes if seed dispersers are absent or unable to disperse their seeds. We investigated dispersal limitation for the large‐seeded tree Virola surinamensis in a human‐modified landscape in southern Costa Rica. During two fruiting seasons, we monitored crop size, seed removal rates, the number of fruiting conspecifics within 100 m, and feeding visitation rates by frugivores at trees located in high and low forest disturbance conditions. Seed removal rates and the total number of seeds removed were high regardless of the disturbance level, but these parameters increased with tree crop size and decreased with the number of fruiting V. surinamensis trees within a 100 m radius. Trees at low disturbance levels were more likely to be visited by seed dispersers. Black mandibled toucans (Ramphastos ambiguus) and spider monkeys (Ateles geoffroyi) were the most important seed dispersers, based on visitation patterns and seed removal rates. Spider monkey feeding visits were more frequent at high disturbance levels, but the monkeys preferentially visited isolated trees with large yields and surrounded by a low number of fruiting Virola trees within 100 m. Toucan visitation patterns were not constrained by any of the predictors and they visited trees equally across the landscape. We suggest that isolated and highly fecund Virola trees are an important food resource for spider monkeys in human‐modified landscapes and that toucans can provide resilience against seed dispersal limitations for large‐seeded plants in human‐modified landscapes in the absence of hunting.     

Carbon dynamics,net primary productivity and human‐appropriated net primary productivity across a forest–cocoa farm landscape in West Africa

Terrestrial net primary productivity (NPP) is an important metric of ecosystem functioning; however, there are little empirical data on the NPP of human‐modified ecosystems, particularly smallholder, perennial crops like cocoa (Theobroma cacao), which are extensive across the tropics. Human‐appropriated NPP (HANPP) is a measure of the proportion of a natural system's NPP that has either been reduced through land‐use change or harvested directly and, previously, has been calculated to estimate the scale of the human impact on the biosphere. Additionally, human modification can create shifts in NPP allocation and decomposition, with concomitant impacts on the carbon cycle. This study presents the results of 3 years of intensive monitoring of forest and smallholder cocoa farms across disturbance, management intensity, distance from forest and farm age gradients. We measured among the highest reported NPP values in tropical forest, 17.57 ± 2.1 and 17.7 ± 1.6 Mg C ha^?1 year^?1 for intact and logged forest, respectively; however, the average NPP of cocoa farms was still higher, 18.8 ± 2.5 Mg C ha^?1 year^?1, which we found was driven by cocoa pod production. We found a dramatic shift in litterfall residence times, where cocoa leaves decomposed more slowly than forest leaves and shade tree litterfall decomposed considerably faster, indicating significant changes in rates of nutrient cycling. The average HANPP value for all cocoa farms was 2.1 ± 1.1 Mg C ha^?1 year^?1; however, depending on the density of shade trees, it ranged from ?4.6 to 5.2 Mg C ha^?1 year^?1. Therefore, rather than being related to cocoa yield, HANPP was reduced by maintaining higher shade levels. Across our monitored farms, 18.9% of farm NPP was harvested (i.e., whole cocoa pods) and only 1.1% (i.e., cocoa beans) was removed from the system, suggesting that the scale of HANPP in smallholder cocoa agroforestry systems is relatively small.     

Combined hybridization capture and shotgun sequencing for ancient DNA analysis of extinct wild and domestic dromedary camel

The performance of hybridization capture combined with next‐generation sequencing (NGS) has seen limited investigation with samples from hot and arid regions until now. We applied hybridization capture and shotgun sequencing to recover DNA sequences from bone specimens of ancient‐domestic dromedary (Camelus dromedarius) and its extinct ancestor, the wild dromedary from Jordan, Syria, Turkey and the Arabian Peninsula, respectively. Our results show that hybridization capture increased the percentage of mitochondrial DNA (mtDNA) recovery by an average 187‐fold and in some cases yielded virtually complete mitochondrial (mt) genomes at multifold coverage in a single capture experiment. Furthermore, we tested the effect of hybridization temperature and time by using a touchdown approach on a limited number of samples. We observed no significant difference in the number of unique dromedary mtDNA reads retrieved with the standard capture compared to the touchdown method. In total, we obtained 14 partial mitochondrial genomes from ancient‐domestic dromedaries with 17–95% length coverage and 1.27–47.1‐fold read depths for the covered regions. Using whole‐genome shotgun sequencing, we successfully recovered endogenous dromedary nuclear DNA (nuDNA) from domestic and wild dromedary specimens with 1–1.06‐fold read depths for covered regions. Our results highlight that despite recent methodological advances, obtaining ancient DNA (aDNA) from specimens recovered from hot, arid environments is still problematic. Hybridization protocols require specific optimization, and samples at the limit of DNA preservation need multiple replications of DNA extraction and hybridization capture as has been shown previously for Middle Pleistocene specimens.