Genetic impacts of Anacapa deer mice reintroductions following rat eradication

The Anacapa deer mouse is an endemic subspecies that inhabits Anacapa Island, part of Channel Islands National Park, California. We used mitochondrial DNA cytochrome c oxidase subunit II gene (COII) and 10 microsatellite loci to evaluate the levels of genetic differentiation and variation in ~1400 Anacapa deer mice sampled before and for 4 years after a black rat (Rattus rattus) eradication campaign that included trapping, captive holding and reintroduction of deer mice. Both mitochondrial and microsatellite analyses indicated significant differentiation between Anacapa deer mice and mainland mice, and genetic variability of mainland mice was significantly higher than Anacapa mice even prior to reintroduction. Bayesian cluster analysis and Principal Coordinates Analysis indicated that East, Middle and West Anacapa mice were genetically differentiated from each other, but translocation of mice among islands resulted in the East population becoming less distinct as a result of management. Levels of heterozygosity were similar before and after management. However, numerous private alleles in the founder populations were not observed after reintroduction and shifts in allele frequencies occurred, indicating that the reintroduced populations experienced substantial genetic drift. Surprisingly, two mitochondrial haplotypes observed in an earlier study of Anacapa deer mice were lost in the 20 years prior to the rat eradication program, leaving only a single haplotype in Anacapa deer mice. This study demonstrates how genetic monitoring can help to understand the re-establishment of endemic species after the eradication of invasive species and to evaluate the effectiveness of the management strategies employed.     

Phylogeography, genetic structure and population divergence time of cheetahs in Africa and Asia: evidence for long-term geographic isolates

The cheetah (Acinonyx jubatus) has been described as a species with low levels of genetic variation. This has been suggested to be the consequence of a demographic bottleneck 10 000–12 000 years ago (ya) and also led to the assumption that only small genetic differences exist between the described subspecies. However, analysing mitochondrial DNA and microsatellites in cheetah samples from most of the historic range of the species we found relatively deep phylogeographic breaks between some of the investigated populations, and most of the methods assessed divergence time estimates predating the postulated bottleneck. Mitochondrial DNA monophyly and overall levels of genetic differentiation support the distinctiveness of Northern‐East African cheetahs (Acinonyx jubatus soemmeringii). Moreover, combining archaeozoological and contemporary samples, we show that Asiatic cheetahs (Acinonyx jubatus venaticus) are unambiguously separated from African subspecies. Divergence time estimates from mitochondrial and nuclear data place the split between Asiatic and Southern African cheetahs (Acinonyx jubatus jubatus) at 32 000–67 000 ya using an average mammalian microsatellite mutation rate and at 4700–44 000 ya employing human microsatellite mutation rates. Cheetahs are vulnerable to extinction globally and critically endangered in their Asiatic range, where the last 70–110 individuals survive only in Iran. We demonstrate that these extant Iranian cheetahs are an autochthonous monophyletic population and the last representatives of the Asiatic subspecies A. j. venaticus. We advocate that conservation strategies should consider the uncovered independent evolutionary histories of Asiatic and African cheetahs, as well as among some African subspecies. This would facilitate the dual conservation priorities of maintaining locally adapted ecotypes and genetic diversity.     

From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal

Defining the scale of connectivity among marine populations and identifying the barriers to gene flow are tasks of fundamental importance for understanding the genetic structure of populations and for the design of marine reserves. Here, we investigated the population genetic structure at three spatial scales of the red gorgonian Paramuricea clavata (Cnidaria, Octocorallia), a key species dwelling in the coralligenous assemblages of the Mediterranean Sea. Colonies of P. clavata were collected from 39 locations across the Mediterranean Sea from Morocco to Turkey and analysed using microsatellite loci. Within three regions (Medes, Marseille and North Corsica), sampling was obtained from multiple locations and at different depths. Three different approaches (measures of genetic differentiation, Bayesian clustering and spatially explicit maximum‐difference algorithm) were used to determine the pattern of genetic structure. We identified genetic breaks in the spatial distribution of genetic diversity, which were concordant with oceanographic conditions in the Mediterranean Sea. We revealed a high level of genetic differentiation among populations and a pattern of isolation by distance across the studied area and within the three regions, underlining short effective larval dispersal in this species. We observed genetic differentiation among populations in the same locality dwelling at different depths, which may be explained by local oceanographic conditions and which may allow a process of local adaptation of the populations to their environment. We discuss the implications of our results for the conservation of the species, which is exposed to various threats.     

Bayesian inference of a historical bottleneck in a heavily exploited marine mammal

Emerging Bayesian analytical approaches offer increasingly sophisticated means of reconstructing historical population dynamics from genetic data, but have been little applied to scenarios involving demographic bottlenecks. Consequently, we analysed a large mitochondrial and microsatellite dataset from the Antarctic fur seal Arctocephalus gazella, a species subjected to one of the most extreme examples of uncontrolled exploitation in history when it was reduced to the brink of extinction by the sealing industry during the late eighteenth and nineteenth centuries. Classical bottleneck tests, which exploit the fact that rare alleles are rapidly lost during demographic reduction, yielded ambiguous results. In contrast, a strong signal of recent demographic decline was detected using both Bayesian skyline plots and Approximate Bayesian Computation, the latter also allowing derivation of posterior parameter estimates that were remarkably consistent with historical observations. This was achieved using only contemporary samples, further emphasizing the potential of Bayesian approaches to address important problems in conservation and evolutionary biology.     

The imprecision of heterozygosity-fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species

In nonpedigreed wild populations, inbreeding depression is often quantified through the use of heterozygosity-fitness correlations (HFCs), based on molecular estimates of relatedness. Although such correlations are typically interpreted as evidence of inbreeding depression, by assuming that the marker heterozygosity is a proxy for genome-wide heterozygosity, theory predicts that these relationships should be difficult to detect. Until now, the vast majority of empirical research in this area has been performed on generally outbred, nonbottlenecked populations, but differences in population genetic processes may limit extrapolation of results to threatened populations. Here, we present an analysis of HFCs, and their implications for the interpretation of inbreeding, in a free-ranging pedigreed population of a bottlenecked species: the endangered takahe (Porphyrio hochstetteri). Pedigree-based inbreeding depression has already been detected in this species. Using 23 microsatellite loci, we observed only weak evidence of the expected relationship between multilocus heterozygosity and fitness at individual life-history stages (such as survival to hatching and fledging), and parameter estimates were imprecise (had high error). Furthermore, our molecular data set could not accurately predict the inbreeding status of individuals (as 'inbred' or 'outbred', determined from pedigrees), nor could we show that the observed HFCs were the result of genome-wide identity disequilibrium. These results may be attributed to high variance in heterozygosity within inbreeding classes. This study is an empirical example from a free-ranging endangered species, suggesting that even relatively large numbers (>20) of microsatellites may give poor precision for estimating individual genome-wide heterozygosity. We argue that pedigree methods remain the most effective method of quantifying inbreeding in wild populations, particularly those that have gone through severe bottlenecks.     

Individual-based analysis opens new insights into understanding population structure and animal behaviour

Studying the movement of individuals in the wild has always been a challenge in ecology. However, estimating such movement is essential in life sciences as it is the base-line for evaluating connectivity, a major component in developing management and conservation plans. Furthermore, movement, or migration, is an essential parameter in population genetics, as it directly affects genetic differentiation. The development of highly variable markers has allowed genetic discrimination between individuals within populations and at larger scales, and the availability of high-throughput technologies means that many samples and hence many individuals can be screened. These advances mean that we can now use genetic identification for tracking individuals, and hence follow both survival and reproductive output through the life cycle. The paper by Morrissey & Ferguson (2011, this issue) is a demonstration of this new capability, as authors were able to infer the movement of salmonid fish initially captured as juveniles, and later as reproductively mature adults.     

Genetic variation in a tropical tree species influences the associated epiphytic plant and invertebrate communities in a complex forest ecosystem

Genetic differences among tree species, their hybrids and within tree species are known to influence associated ecological communities and ecosystem processes in areas of limited species diversity. The extent to which this same phenomenon occurs based on genetic variation within a single tree species, in a diverse complex ecosystem such as a tropical forest, is unknown. The level of biodiversity and complexity of the ecosystem may reduce the impact of a single tree species on associated communities. We assessed the influence of within-species genetic variation in the tree Brosimum alicastrum (Moraceae) on associated epiphytic and invertebrate communities in a neotropical rainforest. We found a significant positive association between genetic distance of trees and community difference of the epiphytic plants growing on the tree, the invertebrates living among the leaf litter around the base of the tree, and the invertebrates found on the tree trunk. This means that the more genetically similar trees are host to more similar epiphyte and invertebrate communities. Our work has implications for whole ecosystem conservation management, since maintaining sufficient genetic diversity at the primary producer level will enhance species diversity of other plants and animals.     

Global patterns of fragmentation and connectivity of mammalian carnivore habitat

Although mammalian carnivores are vulnerable to habitat fragmentation and require landscape connectivity, their global patterns of fragmentation and connectivity have not been examined. We use recently developed high-resolution habitat suitability models to conduct comparative analyses and to identify global hotspots of fragmentation and connectivity for the world's terrestrial carnivores. Species with less fragmentation (i.e. more interior high-quality habitat) had larger geographical ranges, a greater proportion of habitat within their range, greater habitat connectivity and a lower risk of extinction. Species with higher connectivity (i.e. less habitat isolation) also had a greater proportion of high-quality habitat, but had smaller, not larger, ranges, probably reflecting shorter distances between habitat patches for species with restricted distributions; such species were also more threatened, as would be expected given the negative relationship between range size and extinction risk. Fragmentation and connectivity did not differ among Carnivora families, and body mass was associated with connectivity but not fragmentation. On average, only 54.3 per cent of a species' geographical range comprised high-quality habitat, and more troubling, only 5.2 per cent of the range comprised such habitat within protected areas. Identification of global hotspots of fragmentation and connectivity will help guide strategic priorities for carnivore conservation.     

Global habitat suitability models of terrestrial mammals

Detailed large-scale information on mammal distribution has often been lacking, hindering conservation efforts. We used the information from the 2009 IUCN Red List of Threatened Species as a baseline for developing habitat suitability models for 5027 out of 5330 known terrestrial mammal species, based on their habitat relationships. We focused on the following environmental variables: land cover, elevation and hydrological features. Models were developed at 300 m resolution and limited to within species' known geographical ranges. A subset of the models was validated using points of known species occurrence. We conducted a global, fine-scale analysis of patterns of species richness. The richness of mammal species estimated by the overlap of their suitable habitat is on average one-third less than that estimated by the overlap of their geographical ranges. The highest absolute difference is found in tropical and subtropical regions in South America, Africa and Southeast Asia that are not covered by dense forest. The proportion of suitable habitat within mammal geographical ranges correlates with the IUCN Red List category to which they have been assigned, decreasing monotonically from Least Concern to Endangered. These results demonstrate the importance of fine-resolution distribution data for the development of global conservation strategies for mammals.     

Ecology and evolution of mammalian biodiversity

Mammals have incredible biological diversity, showing extreme flexibility in eco-morphology, physiology, life history and behaviour across their evolutionary history. Undoubtedly, mammals play an important role in ecosystems by providing essential services such as regulating insect populations, seed dispersal and pollination and act as indicators of general ecosystem health. However, the macroecological and macroevolutionary processes underpinning past and present biodiversity patterns are only beginning to be explored on a global scale. It is also particularly important, in the face of the global extinction crisis, to understand these processes in order to be able to use this knowledge to prevent future biodiversity loss and loss of ecosystem services. Unfortunately, efforts to understand mammalian biodiversity have been hampered by a lack of data. New data compilations on current species' distributions, ecologies and evolutionary histories now allow an integrated approach to understand this biodiversity. We review and synthesize these new studies, exploring the past and present ecology and evolution of mammalian biodiversity, and use these findings to speculate about the mammals of our future.