Most species are not driven to extinction before genetic factors impact them

There is controversy concerning the role of genetic factors in species extinctions. Many authors have asserted that species are usually driven to extinction before genetic factors have time to impact them, but few studies have seriously addressed this issue. If this assertion is true, there will be little difference in genetic diversity between threatened and taxonomically related nonthreatened species. We compared average heterozygosities in 170 threatened taxa with those in taxonomically related nonthreatened taxa in a comprehensive metaanalysis. Heterozygosity was lower in threatened taxa in 77% of comparisons, a highly significant departure from the predictions of the no genetic impact hypothesis. Heterozygosity was on average 35% lower (median 40%) in threatened taxa than in related nonthreatened ones. These differences in heterozygosity indicate lowered evolutionary potential, compromised reproductive fitness, and elevated extinction risk in the wild. Independent evidence from stochastic computer projections has demonstrated that inbreeding depression elevates extinction risk for threatened species in natural habitats when all other threatening processes are included in the models. Thus, most taxa are not driven to extinction before genetic factors affect them adversely.     

Amphibian and reptile declines over 35 years at La Selva, Costa Rica

Amphibians stand at the forefront of a global biodiversity crisis. More than one-third of amphibian species are globally threatened, and over 120 species have likely suffered global extinction since 1980. Most alarmingly, many rapid declines and extinctions are occurring in pristine sites lacking obvious adverse effects of human activities. The causes of these "enigmatic" declines remain highly contested. Still, lack of long-term data on amphibian populations severely limits our understanding of the distribution of amphibian declines, and therefore the ultimate causes of these declines. Here, we identify a systematic community-wide decline in populations of terrestrial amphibians at La Selva Biological Station, a protected old-growth lowland rainforest in lower Central America. We use data collected over 35 years to show that population density of all species of terrestrial amphibians has declined by approximately 75% since 1970, and we show identical trends for all species of common reptiles. The trends we identify are neither consistent with recent emergence of chytridiomycosis nor the climate-linked epidemic hypothesis, two leading putative causes of enigmatic amphibian declines. Instead, our data suggest that declines are due to climate-driven reductions in the quantity of standing leaf litter, a critical microhabitat for amphibians and reptiles in this assemblage. Our results raise further concerns about the global persistence of amphibian populations by identifying widespread declines in species and habitats that are not currently recognized as susceptible to such risks.     

Latent extinction risk and the future battlegrounds of mammal conservation

Global conservation prioritization usually emphasizes areas with highest species richness or where many species are thought to be at imminent risk of extinction. However, these strategies may overlook areas where many species have biological traits that make them particularly sensitive to future human impact but are not yet threatened because such impact is currently low. In this article, we identify such areas for the world's mammals using latent extinction risk, the discrepancy between a species' current extinction risk and that predicted from models on the basis of biological traits. Species with positive latent risk are currently less threatened than their biology would suggest, usually because they inhabit regions or habitats still comparatively unmodified by human activity. Using large new geographic, biological, and phylogenetic databases for nearly 4,000 mammal species, we map the global geographic distribution of latent risk to reveal areas where the mammal fauna is still relatively unthreatened but has high inherent sensitivity to disturbance. These hotspots include large areas such as the Nearctic boreal forests and tundra that are unrepresented in most current prioritization schemes, as well as high-biodiversity areas such as the island arc from Indonesia to the south Pacific. Incorporating latent extinction risk patterns into conservation planning could help guard against future biodiversity loss by anticipating and preventing species declines before they begin.     

Colloquium paper: are we in the midst of the sixth mass extinction? A view from the world of amphibians

Many scientists argue that we are either entering or in the midst of the sixth great mass extinction. Intense human pressure, both direct and indirect, is having profound effects on natural environments. The amphibians--frogs, salamanders, and caecilians--may be the only major group currently at risk globally. A detailed worldwide assessment and subsequent updates show that one-third or more of the 6,300 species are threatened with extinction. This trend is likely to accelerate because most amphibians occur in the tropics and have small geographic ranges that make them susceptible to extinction. The increasing pressure from habitat destruction and climate change is likely to have major impacts on narrowly adapted and distributed species. We show that salamanders on tropical mountains are particularly at risk. A new and significant threat to amphibians is a virulent, emerging infectious disease, chytridiomycosis, which appears to be globally distributed, and its effects may be exacerbated by global warming. This disease, which is caused by a fungal pathogen and implicated in serious declines and extinctions of >200 species of amphibians, poses the greatest threat to biodiversity of any known disease. Our data for frogs in the Sierra Nevada of California show that the fungus is having a devastating impact on native species, already weakened by the effects of pollution and introduced predators. A general message from amphibians is that we may have little time to stave off a potential mass extinction.     

Multiple ecological pathways to extinction in mammals

As human population and resource demands continue to grow, biodiversity conservation has never been more critical. About one-quarter of all mammals are in danger of extinction, and more than half of all mammal populations are in decline. A major priority for conservation science is to understand the ecological traits that predict extinction risk and the interactions among those predictors that make certain species more vulnerable than others. Here, using a new database of nearly 4,500 mammal species, we use decision-tree models to quantify the multiple interacting factors associated with extinction risk. We show that the correlates of extinction risk vary widely across mammals and that there are unique pathways to extinction for species with different lifestyles and combinations of traits. We find that risk is relative and that all kinds of mammals, across all body sizes, can be at risk depending on their specific ecologies. Our results increase the understanding of extinction processes, generate simple rules of thumb that identify species at greatest risk, and highlight the potential of decision-tree analyses to inform conservation efforts.     

Circuit theory predicts gene flow in plant and animal populations

Maintaining connectivity for broad-scale ecological processes like dispersal and gene flow is essential for conserving endangered species in fragmented landscapes. However, determining which habitats should be set aside to promote connectivity has been difficult because existing models cannot incorporate effects of multiple pathways linking populations. Here, we test an ecological connectivity model that overcomes this obstacle by borrowing from electrical circuit theory. The model vastly improves gene flow predictions because it simultaneously integrates all possible pathways connecting populations. When applied to data from threatened mammal and tree species, the model consistently outperformed conventional gene flow models, revealing that barriers were less important in structuring populations than previously thought. Circuit theory now provides the best-justified method to bridge landscape and genetic data, and holds much promise in ecology, evolution, and conservation planning.     

Extinction risks of Amazonian plant species

Estimates of the number, and preferably the identity, of species that will be threatened by land-use change and habitat loss are an invaluable tool for setting conservation priorities. Here, we use collections data and ecoregion maps to generate spatially explicit distributions for more than 40,000 vascular plant species from the Amazon basin (representing more than 80% of the estimated Amazonian plant diversity). Using the distribution maps, we then estimate the rates of habitat loss and associated extinction probabilities due to land-use changes as modeled under 2 disturbance scenarios. We predict that by 2050, human land-use practices will have reduced the habitat available to Amazonian plant species by ≈12–24%, resulting in 5–9% of species becoming “committed to extinction,” significantly fewer than other recent estimates. Contrary to previous studies, we find that the primary determinant of habitat loss and extinction risk is not the size of a species'' range, but rather its location. The resulting extinction risk estimates are a valuable conservation tool because they indicate not only the total percentage of Amazonian plant species threatened with extinction but also the degree to which individual species and habitats will be affected by current and future land-use changes.     

Ecological basis of extinction risk in birds: habitat loss versus human persecution and introduced predators

Understanding the ecological mechanisms that underlie extinction is fundamental to conservation. It is well established that not all taxa are equally vulnerable to extinction, but the reasons for these differences are poorly understood. This may be, in part, because different taxa are threatened by different mechanisms. Theoretically, sources of extinction risk that perturb the balance between fecundity and longevity, such as human persecution and introduced predators, should be particularly hazardous for taxa that have slow rates of population growth. In contrast, sources of extinction risk that reduce niche availability, such as habitat loss, should represent a particular threat to taxa that are ecologically specialized. Here we test these predictions by using a phylogenetic comparative method and a database on 95 families of birds. As theory predicts, extinction risk incurred through persecution and introduced predators is associated with large body size and long generation time but is not associated with degree of specialization, whereas extinction risk incurred through habitat loss is associated with habitat specialization and small body size but not with generation time. These results demonstrate the importance of considering separately the multiple mechanisms that underlie contemporary patterns of extinction. They also reveal why it has previously proven so difficult to identify simple ecological correlates of overall extinction risk.     

The inflated significance of neutral genetic diversity in conservation genetics

The current rate of species extinction is rapidly approaching unprecedented highs, and life on Earth presently faces a sixth mass extinction event driven by anthropogenic activity, climate change, and ecological collapse. The field of conservation genetics aims at preserving species by using their levels of genetic diversity, usually measured as neutral genome-wide diversity, as a barometer for evaluating population health and extinction risk. A fundamental assumption is that higher levels of genetic diversity lead to an increase in fitness and long-term survival of a species. Here, we argue against the perceived importance of neutral genetic diversity for the conservation of wild populations and species. We demonstrate that no simple general relationship exists between neutral genetic diversity and the risk of species extinction. Instead, a better understanding of the properties of functional genetic diversity, demographic history, and ecological relationships is necessary for developing and implementing effective conservation genetic strategies.     

Invasive hybrid tiger salamander genotypes impact native amphibians

Although the ecological consequences of species invasions are well studied, the ecological impacts of genetic introgression through hybridization are less understood. This is particularly true of the impacts of hybridization on “third party” community members not genetically involved in hybridization. We also know little about how direct interactions between hybrid and parental individuals influence fitness. Here, we examined the ecological effects of hybridization between the native, threatened California Tiger Salamander (Ambystoma californiense) and the introduced Barred Tiger Salamander (Ambystoma tigrinum mavortium). Native x introduced hybrids are widespread in California, where they are top predators in seasonal ponds. We examined the impacts of early generation hybrids (first 2 generations of parental crosses) and contemporary hybrids derived from ponds where hybrids have been under selection in the wild for 20 generations. We found that most classes of hybrid tiger salamander larvae dramatically reduced survival of 2 native community members, the Pacific Chorus Frog (Pseudacris regilla) and the California Newt (Taricha torosa). We also found that native A. californiense larvae were negatively impacted by the presence of hybrid larvae: Native survival and size at metamorphosis were reduced and time to metamorphosis was extended. We also observed a large influence of Mendelian dominance on size, metamorphic timing and predation rate of hybrid tiger salamanders. These results suggest that both genetic and ecological factors are likely to influence the dynamics of admixture, and that tiger salamander hybridization might constitute a threat to additional pond-breeding species of concern in the region.     

Thousand-year-long Chinese time series reveals climatic forcing of decadal locust dynamics

For >1,000 years, Chinese officials have recorded the annual abundance of the oriental migratory locust Locusta migratoria manilensis, with the ultimate aim of predicting locust outbreaks. Linking these records with temperature and precipitation reconstructions for the period 957-1956, we show that decadal mean locust abundance is highest during cold and wet periods. These periods coincide with above-average frequencies of both floods and droughts in the lower Yangtze River, phenomena that are associated with locust outbreaks. Our results imply differential ecological responses to interdecadal and interannual climatic variability. Such frequency-dependent effects deserve increased attention in global warming studies.     

Diversity components of impending primate extinctions

Many extant species are at risk to go extinct. This impending loss of species is likely to cause changes in future ecosystem functions. Ecological components of diversity, such as dietary or habitat specializations, can be used to estimate the impact of extinctions on ecosystem functions. As an approach to estimate the impact of future extinctions, we tested interdependency between ecological and taxonomic change based on current predictions of extinction rates in primates. We analyzed the ecological characteristics of extant primate faunas having species in various categories of endangerment of extinction and forecasted the future primate faunas as if they were paleontological faunas. Predicting future faunas combines the wealth of ecological information on living primates with large, fossil record-like changes in diversity. Predicted extinction patterns of living primates in Africa, Asia, Madagascar, and South America show that changes in ecology differ among the regions in ways that are not reducible to taxonomic measures. The ecological effects of primate extinctions are initially least severe in South America and larger in Asia and Africa. Disproportionately larger ecological changes are projected for Madagascar. The use of taxonomy as a proxy for ecology can mislead when estimating competence of future primate ecosystems.     

The effect of geographic range on extinction risk during background and mass extinction

Wide geographic range is generally thought to buffer taxa against extinction, but the strength of this effect has not been investigated for the great majority of the fossil record. Although the majority of genus extinctions have occurred between major mass extinctions, little is known about extinction selectivity regimes during these "background" intervals. Consequently, the question of whether selectivity regimes differ between background and mass extinctions is largely unresolved. Using logistic regression, we evaluated the selectivity of genus survivorship with respect to geographic range by using a global database of fossil benthic marine invertebrates spanning the Cambrian through the Neogene periods, an interval of approximately 500 My. Our results show that wide geographic range has been significantly and positively associated with survivorship for the great majority of Phanerozoic time. Moreover, the significant association between geographic range and survivorship remains after controlling for differences in species richness and abundance among genera. However, mass extinctions and several second-order extinction events exhibit less geographic range selectivity than predicted by range alone. Widespread environmental disturbance can explain the reduced association between geographic range and extinction risk by simultaneously affecting genera with similar ecological and physiological characteristics on global scales. Although factors other than geographic range have certainly affected extinction risk during many intervals, geographic range is likely the most consistently significant predictor of extinction risk in the marine fossil record.     

Spatial synchrony of local populations has increased in association with the recent Northern Hemisphere climate trend

According to ecological theory, populations whose dynamics are entrained by environmental correlation face increased extinction risk as environmental conditions become more synchronized spatially. This prediction is highly relevant to the study of ecological consequences of climate change. Recent empirical studies have indicated, for example, that large-scale climate synchronizes trophic interactions and population dynamics over broad spatial scales in freshwater and terrestrial systems. Here, we present an analysis of century-scale, spatially replicated data on local weather and the population dynamics of caribou in Greenland. Our results indicate that spatial autocorrelation in local weather has increased with large-scale climatic warming. This increase in spatial synchrony of environmental conditions has been matched, in turn, by an increase in the spatial synchrony of local caribou populations toward the end of the 20th century. Our results indicate that spatial synchrony in environmental conditions and the populations influenced by them are highly variable through time and can increase with climatic warming. We suggest that if future warming can increase population synchrony, it may also increase extinction risk.     

Complementary sex determination substantially increases extinction proneness of haplodiploid populations

The role of genetic factors in extinction is firmly established for diploid organisms, but haplodiploids have been considered immune to genetic load impacts because deleterious alleles are readily purged in haploid males. However, we show that single-locus complementary sex determination ancestral to the haplodiploid Hymenoptera (ants, bees, and wasps) imposes a substantial genetic load through homozygosity at the sex locus that results in the production of inviable or sterile diploid males. Using stochastic modeling, we have discovered that diploid male production (DMP) can initiate a rapid and previously uncharacterized extinction vortex. The extinction rate in haplodiploid populations with DMP is an order of magnitude greater than in its absence under realistic but conservative demographic parameter values. Furthermore, DMP alone can elevate the base extinction risk in haplodiploids by over an order of magnitude higher than that caused by inbreeding depression in threatened diploids. Thus, contrary to previous expectations, haplodiploids are more, rather than less, prone to extinction for genetic reasons. Our findings necessitate a fundamental shift in approaches to the conservation and population biology of these ecologically and economically crucial insects.     

Recent ecological responses to climate change support predictions of high extinction risk

Predicted effects of climate change include high extinction risk for many species, but confidence in these predictions is undermined by a perceived lack of empirical support. Many studies have now documented ecological responses to recent climate change, providing the opportunity to test whether the magnitude and nature of recent responses match predictions. Here, we perform a global and multitaxon metaanalysis to show that empirical evidence for the realized effects of climate change supports predictions of future extinction risk. We use International Union for Conservation of Nature (IUCN) Red List criteria as a common scale to estimate extinction risks from a wide range of climate impacts, ecological responses, and methods of analysis, and we compare predictions with observations. Mean extinction probability across studies making predictions of the future effects of climate change was 7% by 2100 compared with 15% based on observed responses. After taking account of possible bias in the type of climate change impact analyzed and the parts of the world and taxa studied, there was less discrepancy between the two approaches: predictions suggested a mean extinction probability of 10% across taxa and regions, whereas empirical evidence gave a mean probability of 14%. As well as mean overall extinction probability, observations also supported predictions in terms of variability in extinction risk and the relative risk associated with broad taxonomic groups and geographic regions. These results suggest that predictions are robust to methodological assumptions and provide strong empirical support for the assertion that anthropogenic climate change is now a major threat to global biodiversity.     

Selectivity of terrestrial gastropod extinctions on an oceanic archipelago and insights into the anthropogenic extinction process

Anthropogenic impacts have led to widespread extinctions of species on oceanic islands but the nature of many of these extinctions remains poorly known. Here we investigate extinction selectivities of terrestrial gastropods from the Ogasawara archipelago in the northwest Pacific, where anthropogenic threats have changed over time, shifting primarily from the effects of habitat loss to predation by a variety of different predators. Across all of the islands, extinct species had significantly smaller geographic ranges compared with species that are still alive, but among the surviving species, ranges of those that are currently declining due to human impacts do not differ significantly from those that are not threatened. Extinctions were selective with respect to spire index (SI) of shells, a trait of potential functional importance, but the relationship between body size and extinction vulnerability varied among extinction agents, some of which were strongly size selective, whereas others were not. Overall, whereas anthropogenic impacts have resulted in nonrandom losses of phenotypic diversity, the patterns of selectivity are complex, vary among islands, and with the type of threat. As extinction agents have changed historically, so has the pattern of loss. Because of the changing nature of anthropogenic impacts, resiliency to one type of threat does not guarantee long-term survival of species and future patterns of biodiversity loss on these islands are likely to be different from those in the past.     

Dynamics of an emerging disease drive large-scale amphibian population extinctions

Epidemiological theory generally suggests that pathogens will not cause host extinctions because the pathogen should fade out when the host population is driven below some threshold density. An emerging infectious disease, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) is directly linked to the recent extinction or serious decline of hundreds of amphibian species. Despite continued spread of this pathogen into uninfected areas, the dynamics of the host–pathogen interaction remain unknown. We use fine-scale spatiotemporal data to describe (i) the invasion and spread of Bd through three lake basins, each containing multiple populations of the mountain yellow-legged frog, and (ii) the accompanying host–pathogen dynamics. Despite intensive sampling, Bd was not detected on frogs in study basins until just before epidemics began. Following Bd arrival in a basin, the disease spread to neighboring populations at ≈700 m/yr in a wave-like pattern until all populations were infected. Within a population, infection prevalence rapidly reached 100% and infection intensity on individual frogs increased in parallel. Frog mass mortality began only when infection intensity reached a critical threshold and repeatedly led to extinction of populations. Our results indicate that the high growth rate and virulence of Bd allow the near-simultaneous infection and buildup of high infection intensities in all host individuals; subsequent host population crashes therefore occur before Bd is limited by density-dependent factors. Preventing infection intensities in host populations from reaching this threshold could provide an effective strategy to avoid the extinction of susceptible amphibian species in the wild.     

Declines of biomes and biotas and the future of evolution

Although panel discussants disagreed whether the biodiversity crisis constitutes a mass extinction event, all agreed that current extinction rates are 50-500 times background and are increasing and that the consequences for the future evolution of life are serious. In response to the on-going rapid decline of biomes and homogenization of biotas, the panelists predicted changes in species geographic ranges, genetic risks of extinction, genetic assimilation, natural selection, mutation rates, the shortening of food chains, the increase in nutrient-enriched niches permitting the ascendancy of microbes, and the differential survival of ecological generalists. Rates of evolutionary processes will change in different groups, and speciation in the larger vertebrates is essentially over. Action taken over the next few decades will determine how impoverished the biosphere will be in 1,000 years when many species will suffer reduced evolvability and require interventionist genetic and ecological management. Whether the biota will continue to provide the dependable ecological services humans take for granted is less clear. The discussants offered recommendations, including two of paramount importance (concerning human populations and education), seven identifying specific scientific activities to better equip us for stewardship of the processes of evolution, and one suggesting that such stewardship is now our responsibility. The ultimate test of evolutionary biology as a science is not whether it solves the riddles of the past but rather whether it enables us to manage the future of the biosphere. Our inability to make clearer predictions about the future of evolution has serious consequences for both biodiversity and humanity.     

An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle

Many pathogens, such as the agents of West Nile encephalitis and plague, are maintained in nature by animal reservoirs and transmitted to humans by arthropod vectors. Efforts to reduce disease incidence usually rely on vector control or immunization of humans. Lyme disease, for which no human vaccine is currently available, is a commonly reported vector-borne disease in North America and Europe. In a recently developed, ecological approach to disease prevention, we intervened in the natural cycle of the Lyme disease agent (Borrelia burgdorferi) by immunizing wild white-footed mice (Peromyscus leucopus), a reservoir host species, with either a recombinant antigen of the pathogen, outer surface protein A, or a negative control antigen in a repeated field experiment with paired experimental and control grids stratified by site. Outer surface protein A vaccination significantly reduced the prevalence of B. burgdorferi in nymphal blacklegged ticks (Ixodes scapularis) collected at the sites the following year in both experiments. The magnitude of the vaccine's effect at a given site correlated with the tick infection prevalence found on the control grid, which in turn correlated with mouse density. These data, as well as differences in the population structures of B. burgdorferi in sympatric ticks and mice, indicated that nonmouse hosts contributed more to infecting ticks than previously expected. Thus, where nonmouse hosts play a large role in infection dynamics, vaccination should be directed at additional species.