Phylogenetic Comparative Methods Strengthen Evidence for Reduced Genetic Diversity among Endangered Tetrapods

Abstract: The fitness of species with little genetic diversity is expected to be affected by inbreeding and an inability to respond to environmental change. Conservation theory suggests that endangered species will generally demonstrate lower genetic diversity than taxa that are not threatened. This hypothesis has been challenged because the time frame of anthropogenic extinction may be too fast to expect genetic factors to significantly contribute. I conducted a meta‐analysis to examine how genetic diversity in 894 tetrapods correlates with extinction threat level. Because species are not evolutionarily independent, I used a phylogenetic regression framework to address this issue. Mean genetic diversity of tetrapods, as assessed by protein heterozygosity, was 29.7–31.5% lower on average in threatened species than in their nonthreatened relatives, a highly significant reduction. Within amphibians as diversity decreased extinction risk increased in phylogenetic models, but not in nonphylogenetic regressions. The effects of threatened status on diversity also remained significant after accounting for body size in mammals. These results support the hypothesis that genetic effects on population fitness are important in the extinction process.     

Effects of Human Activity on Global Extinction Risk

Both natural and anthropogenic factors are important in determining a species' risk of extinction. Little work has been done, however, to quantify the magnitude of current anthropogenic influences on the extinction process. The purpose of this study is to determine the extent to which measures of the intensity of human activity are related to the global variability of two measures of species' susceptibility to extinction. We observed six indices of human activities in 90 countries, and we tested their relationships to the proportion of threatened bird and mammal species in each country, as well as to mammalian population density. After correcting for area effects, latitudinal diversity gradients, and body size (for population density), 28 to 50% of the remaining variation was statistically attributable to anthropogenic variables. Different measures of anthropogenic influence were most closely related to extinction risk in birds and mammals. Human population density was the variable most closely related to the proportion of threatened bird species per country, whereas per capita GNP was more important for mammal species. Mammalian population density strongly correlates with the extent of protected area per country. Contrary to suggestions in earlier literature, our work does not support the hypothesis that habitat loss is a prime contributor to species loss because frequencies of threatened birds and mammals are not closely related to patterns of land use.     

Incorporating Evolutionary Measures into Conservation Prioritization

Abstract:  Conservation prioritization is dominated by the threat status of candidate species. However, species differ markedly in the shared genetic information they embody, and this information is not taken into account if species are prioritized by threat status alone. We developed a system of prioritization that incorporates both threat status and genetic information and applied it to 9546 species of birds worldwide. We devised a simple measure of a species' genetic value that takes into account the shape of the entire taxonomic tree of birds. This measure approximates the evolutionary history that each species embodies and sums to the phylogenetic diversity of the entire taxonomic tree. We then combined this genetic value with each species' probability of extinction to create a species-specific measure of expected loss of genetic information. The application of our methods to the world's avifauna showed that ranking species by expected loss of genetic information may help preserve bird evolutionary history by upgrading those threatened species with fewer close relatives. We recommend developing a mechanism to incorporate a species' genetic value into the prioritization framework.     

Climate Change, Elevational Range Shifts, and Bird Extinctions

Abstract:  Limitations imposed on species ranges by the climatic, ecological, and physiological effects of elevation are important determinants of extinction risk. We modeled the effects of elevational limits on the extinction risk of landbirds, 87% of all bird species. Elevational limitation of range size explained 97% of the variation in the probability of being in a World Conservation Union category of extinction risk. Our model that combined elevational ranges, four Millennium Assessment habitat-loss scenarios, and an intermediate estimate of surface warming of 2.8° C, projected a best guess of 400–550 landbird extinctions, and that approximately 2150 additional species would be at risk of extinction by 2100. For Western Hemisphere landbirds, intermediate extinction estimates based on climate-induced changes in actual distributions ranged from 1.3% (1.1° C warming) to 30.0% (6.4° C warming) of these species. Worldwide, every degree of warming projected a nonlinear increase in bird extinctions of about 100–500 species. Only 21% of the species predicted to become extinct in our scenarios are currently considered threatened with extinction. Different habitat-loss and surface-warming scenarios predicted substantially different futures for landbird species. To improve the precision of climate-induced extinction estimates, there is an urgent need for high-resolution measurements of shifts in the elevational ranges of species. Given the accelerating influence of climate change on species distributions and conservation, using elevational limits in a tested, standardized, and robust manner can improve conservation assessments of terrestrial species and will help identify species that are most vulnerable to global climate change. Our climate-induced extinction estimates are broadly similar to those of bird species at risk from other factors, but these estimates largely involve different sets of species.     

Genetic diversity and IUCN Red List status

The International Union for Conservation of Nature (IUCN) Red List is an important and widely used tool for conservation assessment. The IUCN uses information about a species’ range, population size, habitat quality and fragmentation levels, and trends in abundance to assess extinction risk. Genetic diversity is not considered, although it affects extinction risk. Declining populations are more strongly affected by genetic drift and higher rates of inbreeding, which can reduce the efficiency of selection, lead to fitness declines, and hinder species’ capacities to adapt to environmental change. Given the importance of conserving genetic diversity, attempts have been made to find relationships between red-list status and genetic diversity. Yet, there is still no consensus on whether genetic diversity is captured by the current IUCN Red List categories in a way that is informative for conservation. To assess the predictive power of correlations between genetic diversity and IUCN Red List status in vertebrates, we synthesized previous work and reanalyzed data sets based on 3 types of genetic data: mitochondrial DNA, microsatellites, and whole genomes. Consistent with previous work, species with higher extinction risk status tended to have lower genetic diversity for all marker types, but these relationships were weak and varied across taxa. Regardless of marker type, genetic diversity did not accurately identify threatened species for any taxonomic group. Our results indicate that red-list status is not a useful metric for informing species-specific decisions about the protection of genetic diversity and that genetic data cannot be used to identify threat status in the absence of demographic data. Thus, there is a need to develop and assess metrics specifically designed to assess genetic diversity and inform conservation policy, including policies recently adopted by the UN's Convention on Biological Diversity Kunming-Montreal Global Biodiversity Framework.     

Effects of uncertainty and variability on population declines and IUCN Red List classifications

The International Union for Conservation of Nature (IUCN) Red List Categories and Criteria is a quantitative framework for classifying species according to extinction risk. Population models may be used to estimate extinction risk or population declines. Uncertainty and variability arise in threat classifications through measurement and process error in empirical data and uncertainty in the models used to estimate extinction risk and population declines. Furthermore, species traits are known to affect extinction risk. We investigated the effects of measurement and process error, model type, population growth rate, and age at first reproduction on the reliability of risk classifications based on projected population declines on IUCN Red List classifications. We used an age‐structured population model to simulate true population trajectories with different growth rates, reproductive ages and levels of variation, and subjected them to measurement error. We evaluated the ability of scalar and matrix models parameterized with these simulated time series to accurately capture the IUCN Red List classification generated with true population declines. Under all levels of measurement error tested and low process error, classifications were reasonably accurate; scalar and matrix models yielded roughly the same rate of misclassifications, but the distribution of errors differed; matrix models led to greater overestimation of extinction risk than underestimations; process error tended to contribute to misclassifications to a greater extent than measurement error; and more misclassifications occurred for fast, rather than slow, life histories. These results indicate that classifications of highly threatened taxa (i.e., taxa with low growth rates) under criterion A are more likely to be reliable than for less threatened taxa when assessed with population models. Greater scrutiny needs to be placed on data used to parameterize population models for species with high growth rates, particularly when available evidence indicates a potential transition to higher risk categories.     

Range Size and Extinction Risk in Forest Birds

Abstract:  Small geographical range size is the single best predictor of threat of extinction in terrestrial species. Knowing how small a species' range has to be before authorities consider it threatened with extinction would allow prediction of a species' risk from continued deforestation and warming climates and provide a baseline for conservation and management strategies aspiring to mitigate these threats. To determine the threshold at which forest-dependent bird species become threatened with extinction, we compared the range sizes of threatened and nonthreatened species. In doing so, we present a simple, repeatable, and practical protocol to quantify range size. We started with species' ranges published in field guides or comparable sources. We then trimmed these ranges, that is, we included only those parts of the ranges that met the species' requirements of elevation and types of forest preferred. Finally, we further trimmed the ranges to the amount of forest cover that remains. This protocol generated an estimate of the remaining suitable range for each species. We compared these range estimates with those from the World Conservation Union Red List. We used the smaller of the two estimates to determine the threshold, 11,000 km², below which birds should be considered threatened. Species considered threatened that have larger ranges than this qualified under other (nonspatial) red list criteria. We identified a suite of species (18) that have not yet qualified as threatened but that have perilously small ranges—about 11% of the nonthreatened birds we analyzed. These birds are likely at risk of extinction and reevaluation of their status is urgently needed.     

Erosion of Heterozygosity in Fluctuating Populations

Abstract: Demographic, environmental, and genetic stochasticity threaten the persistence of isolated populations. The relative importance of these intertwining factors remains unresolved, but a common view is that random demographic and environmental events will usually drive small populations to the brink of extinction before genetic deterioration poses a serious threat. To evaluate the potential importance of genetic factors, we analyzed a model linking demographic and environmental conditions to the loss of genetic diversity in isolated populations undergoing natural levels of fluctuation. Nongenetic processes—environmental stochasticity and population demography—were modeled according to a bounded diffusion process. Genetic processes were modeled by quantifying the rate of drift according to the effective population size, which was predicted from the same parameters used to describe the nongenetic processes. We combined these models to predict the heterozygosity remaining at the time of extinction, as predicted by the nongenetic portion of the model. Our model predicts that many populations will lose most or all of their neutral genetic diversity before nongenetic random events lead to extinction. Given the abundant evidence for inbreeding depression and recent evidence for elevated extinction rates of inbred populations, our findings suggest that inbreeding may be a greater general threat to population persistence than is generally recognized. Therefore, conservation biologists should not ignore the genetic component of extinction risk when assessing species endangerment and developing recovery plans.     

Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation

Shrubs and trees are assumed less likely to lose genetic variation in response to habitat fragmentation because they have certain life-history characteristics such as long lifespans and extensive pollen flow. To test this assumption, we conducted a meta-analysis with data on 97 woody plant species derived from 98 studies of habitat fragmentation. We measured the weighted response of four different measures of population-level genetic diversity to habitat fragmentation with Hedge's d and Spearman rank correlation. We tested whether the genetic response to habitat fragmentation was mediated by life-history traits (longevity, pollination mode, and seed dispersal vector) and study characteristics (genetic marker and plant material used). For both tests of effect size habitat fragmentation was associated with a substantial decrease in expected heterozygosity, number of alleles, and percentage of polymorphic loci, whereas the population inbreeding coefficient was not associated with these measures. The largest proportion of variation among effect sizes was explained by pollination mechanism and by the age of the tissue (progeny or adult) that was genotyped. Our primary finding was that wind-pollinated trees and shrubs appeared to be as likely to lose genetic variation as insect-pollinated species, indicating that severe habitat fragmentation may lead to pollen limitation and limited gene flow. In comparison with results of previous meta-analyses on mainly herbaceous species, we found trees and shrubs were as likely to have negative genetic responses to habitat fragmentation as herbaceous species. We also found that the genetic variation in offspring was generally less than that of adult trees, which is evidence of a genetic extinction debt and probably reflects the genetic diversity of the historical, less-fragmented landscape.     

Genetics, Taxonomy, and Conservation of the Threatened California Gnatcatcher

Abstract: The California Gnatcatcher (   Polioptila californica ) has become a flagship species in the dispute over development of southern California's unique coastal sage scrub habitat, a fragile, geographically restricted ecosystem with high endemism. One aspect of the controversy concerns the status of the subspecies of this bird in southern California coastal sage scrub that is currently listed as threatened under the U.S. Endangered Species Act. To investigate the recent population history of this species and the genetic distinctiveness of subspecies and to inform conservation planning, we used direct sequencing of mitochondrial DNA (mtDNA) for 64 individuals from 13 samples taken throughout the species' range. We found that coastal sage scrub populations of California Gnatcatchers are not genetically distinct from populations in Baja California, which are dense and continuously distributed throughout the peninsula. Rather, mtDNA sequences from this species contain the signatures of population growth and support a hypothesis of recent expansion of populations from a southern Baja California refugium northward into the southern coastal regions of California. During this expansion, stochastic events led to a reduction in genetic variation in the newly occupied range. Thus, preservation of coastal sage scrub cannot be linked to maintaining the genetic diversity of northern gnatcatcher populations, despite previous recognition of subspecies. Our study suggests that not all currently recognized subspecies are equivalent to evolutionarily significant units and illustrates the danger of focusing conservation efforts for threatened habitats on a single species.     

Combined effects of life-history traits and human impact on extinction risk of freshwater megafauna

Megafauna species are intrinsically vulnerable to human impact. Freshwater megafauna (i.e., freshwater animals ≥30 kg, including fishes, mammals, reptiles, and amphibians) are subject to intensive and increasing threats. Thirty-four species are listed as critically endangered on the International Union for Conservation of Nature (IUCN). Red List of Threatened Species, the assessments for which are an important basis for conservation actions but remain incomplete for 49 (24%) freshwater megafauna species. Consequently, the window of opportunity for protecting these species could be missed. Identifying the factors that predispose freshwater megafauna to extinction can help predict their extinction risk and facilitate more effective and proactive conservation actions. Thus, we collated 8 life-history traits for 206 freshwater megafauna species. We used generalized linear mixed models to examine the relationships between extinction risk based on the IUCN Red List categories and the combined effect of multiple traits, as well as the effect of human impact on these relationships for 157 classified species. The most parsimonious model included human impact and traits related to species’ recovery potential including life span, age at maturity, and fecundity. Applying the most parsimonious model to 49 unclassified species predicted that 17 of them are threatened. Accounting for model predictions together with IUCN Red List assessments, 50% of all freshwater megafauna species are considered threatened. The Amazon and Yangtze basins emerged as global diversity hotspots of threatened freshwater megafauna, in addition to existing hotspots, including the Ganges-Brahmaputra and Mekong basins and the Caspian Sea region. Assessment and monitoring of those species predicted to be threatened are needed, especially in the Amazon and Yangtze basins. Investigation of life-history traits and trends in population and distribution, regulation of overexploitation, maintaining river connectivity, implementing protected areas focusing on freshwater ecosystems, and integrated basin management are required to protect threatened freshwater megafauna in diversity hotspots.     

Conservation Genetics of Potentially Endangered Mutualisms: Reduced Levels of Genetic Variation in Specialist versus Generalist Bees

Abstract:  Oligolectic bees collect pollen from one or a few closely related species of plants, whereas polylectic bees visit a variety of flowers for pollen. Because of their more restricted range of host plants, it maybe expected that specialists exist in smaller, more isolated populations, with lower effective population sizes than generalists. Consequently, we hypothesized that oligolectic bees have reduced levels of genetic variation relative to related polylectic species. To test this hypothesis, we used five phylogenetically independent pairs of species in which one member was oligolectic and the other was polylectic. We assayed genetic variation in our species pairs at an average of 32 allozyme loci. Within each species pair, the oligolectic member had fewer polymorphic loci, lower average allelic richness, and lower average expected heterozygosity than its polylectic relative. Averaged over all species pairs, this corresponds to a 21% reduction in allelic richness, a 72% reduction in the proportion of polymorphic loci, and an 83% reduction in expected heterozygosity in specialists compared with generalists. Our data support the hypothesis of reduced effective population size in oligolectic bees and suggest that they may be more prone to extinction as a result. We suggest that in instances in which bee specialists are involved in mutually codependent relationships with their floral hosts, these mutualisms may be endangered for genetic and ecological reasons.     

Genetic and demographic consequences of importing animals into a small population: a simulation model of the Texas State Bison Herd (USA)

The extant 40 bison (Bison bison) constituting the Texas State Bison Herd (TSBH; USA) are directly and exclusively descended from a bison herd assembled by Charles Goodnight in the 1880s, representing a historically and genetically valuable resource. The population currently suffers from low genetic variation, low heterozygosity, high calf mortality, and low natality rates compared with other closed bison populations. Population viability analysis using the VORTEX program previously indicated a 99% chance of population extinction within the next 41 years [J. Mamm. 85 (2004) in press]. We developed a stochastic simulation model to evaluate the genetic and demographic consequences of various management scenarios for the TSBH using genotypic data from 51 microsatellite loci and demographic information recorded over a 6-year period. Our results reveal that without the introduction of new genetic variation, approximately 37% of the representative microsatellite loci will become fixed as the TSBH continues to lose genetic variation at a staggering rate of 30–40% within the next 50 years. Furthermore, if the current trends in natality and mortality rates continue, our model indicates the TSBH faces a 99% chance of extinction in the next 51 years. With the importation of unrelated male bison into the TSBH, and under the assumption of increased fitness, the probability of population survival in the next 100 years increases to 100%, and the population will reach the approximate carrying capacity of 200 bison in 15–16 years. Furthermore, our model predicts increases in genetic diversity and heterozygosity of 24.7–48.4% and 17.5–36.5%, respectively, in the next 100 years following the addition of new genetic variation. We conclude that the importation of bison into the TSBH is necessary to prevent extinction and ensure long-term population survival.     

Implications of genetics and current protected areas for conservation of 5 endangered primates in China

Most of China's 24–28 primate species are threatened with extinction. Habitat reduction and fragmentation are perhaps the greatest threats. We used published data from a conservation genetics study of 5 endangered primates in China (Rhinopithecus roxellana, R. bieti, R. brelichi, Trachypithecus francoisi, and T. leucocephalus); distribution data on these species; and the distribution, area, and location of protected areas to inform conservation strategies for these primates. All 5 species were separated into subpopulations with unique genetic components. Gene flow appeared to be strongly impeded by agricultural land, meadows used for grazing, highways, and humans dwellings. Most species declined severely or diverged concurrently as human population and crop land cover increased. Nature reserves were not evenly distributed across subpopulations with unique genetic backgrounds. Certain small subpopulations were severely fragmented and had higher extinction risk than others. Primate mobility is limited and their genetic structure is strong and susceptible to substantial loss of diversity due to local extinction. Thus, to maximize preservation of genetic diversity in all these primate species, our results suggest protection is required for all sub‐populations. Key priorities for their conservation include maintaining R. roxellana in Shennongjia national reserve, subpopulations S4 and S5 of R. bieti and of R. brelichi in Fanjingshan national reserve, subpopulation CGX of T. francoisi in central Guangxi Province, and all 3 T. leucocephalus sub‐populations in central Guangxi Province.     

A Critique of the Recovery of Greenback Cutthroat Trout

Abstract: There are no examples of recovery of fish listed under the U.S. Endangered Species Act, but the number of federally threatened greenback cutthroat trout (  Oncorhynchus clarki stomias ) populations is approaching the delisting goal. We evaluated recovery of this subspecies in light of developing theory in conservation biology and with regard to recovery of other salmonids in the inland western United States. Four of the five criteria used to define populations that would count toward delisting appeared to underestimate the risk of extinction of those populations. Typically, recovery goals for numbers of greenback cutthroat trout populations were less stringent than those for other inland salmonids petitioned for listing or listed as threatened under the Endangered Species Act and were comparable to those for a federally endangered species. Before delisting is considered, we propose that historical populations be replicated in additional waters to protect genetic diversity and that existing populations be enlarged to reduce their vulnerability to demographic variation, to increase their access to refugia, and to permit reestablishment of mobile life histories. Existing stocks should also be evaluated to determine whether they represent distinct population segments.     

Phylogeny-based conservation priorities for Australian freshwater fishes

Conservation scientists are increasingly interested in the question of how extinction prunes the tree of life. This question is particularly important for Australian freshwater fishes because there is a broad mix of ∼300 old and young species, many of which are severely threatened. We used a complete species-level phylogeny of Australian freshwater fishes to examine phylogenetic nonrandomness of extinction risk. We computed the potential loss of phylogenetic diversity by simulating extinction across the tree under a pattern weighted based on International Union for Conservation of Nature extinction risk category and compared this loss to projected diversity loss under a random null model of extinction. Finally, we calculated EDGE (evolutionary distinctiveness, global endangerment) scores for 251 freshwater and 60 brackish species and compiled a list of high-priority species for conservation actions based on their extinction risk and evolutionary uniqueness. Extinction risk was not random and was clustered in both diversity cradles (recently diversifying, species-rich clades, such as Galaxiidae and Percichthyidae) and museums (older, species-poor groups, such as freshwater chondrichthyans). Clustered extinction made little difference to the average expected loss of phylogenetic diversity. However, the upper bound of loss was higher under a selective model of extinction, particularly when the counts of species lost were low. Thus, the loss of highly threatened species would diminish the tree of life more than a null model of randomly distributed extinction.  High priority species included both widely recognized and charismatic ones, such as the Queensland lungfish (Neoceratodus forsteri), river sharks, and freshwater sawfishes, and lesser-known species that receive less public attention, including the salamanderfish (Lepidogalaxias salamandroides), cave gudgeons, and many galaxiids, rainbowfishes, and pygmy perches.     

Conserving the abundance of nonthreatened species

Human modification of the environment is driving declines in population size and distributional extent of much of the world's biota. These declines extend to many of the most abundant and widespread species, for which proportionally small declines can result in the loss of vast numbers of individuals, biomass, and interactions. These losses could have major localized effects on ecological and cultural processes and services without elevating a species’ global extinction risk. Although most conservation effort is directed at species threatened with extinction in the very near term, the value of retaining abundance regardless of global extinction risk is justifiable based on many biodiversity or ecosystem service metrics, including cultural services, at scales from local to global. The challenges of identifying conservation priorities for widespread and abundant species include quantifying the effects of species’ abundance on services and understanding how these effects are realized as populations decline. Negative effects of population declines may be disconnected from the threat processes driving declines because of species movements and environment flows (e.g., hydrology). Conservation prioritization for these species shares greater similarity with invasive species risk assessments than extinction risk assessments because of the importance of local context and per capita effects of abundance on other species. Because conservation priorities usually focus on preventing the extinction of threatened species, the rationale and objectives for incorporating declines of nonthreatened species must be clearly articulated, going beyond extinction risk to encompass the range of likely harmful effects (e.g., secondary extinctions, loss of ecosystem services) if declines persist or are not reversed. Research should focus on characterizing the effects of local declines in species that are not threatened globally across a range of ecosystem services and quantifying the spatial distribution of these effects through the distribution of abundance. The case for conserving abundance in nonthreatened species can be made most powerfully when the costs of losing this abundance are better understood.     

Benefits to poorly studied taxa of conservation of bird and mammal diversity on islands

Protected area delineation and conservation action are urgently needed on marine islands, but the potential biodiversity benefits of these activities can be difficult to assess due to lack of species diversity information for lesser known taxa. We used linear mixed effects modeling and simple spatial analyses to investigate whether conservation activities based on the diversity of well‐known insular taxa (birds and mammals) are likely to also capture the diversity of lesser known taxa (reptiles, amphibians, vascular land plants, ants, land snails, butterflies, and tenebrionid beetles). We assembled total, threatened, and endemic diversity data for both well‐known and lesser known taxa and combined these with physical island biogeography characteristics for 1190 islands from 109 archipelagos. Among physical island biogeography factors, island area was the best indicator of diversity of both well‐known and little‐known taxa. Among taxonomic factors, total mammal species richness was the best indicator of total diversity of lesser known taxa, and the combination of threatened mammal and threatened bird diversity was the best indicator of lesser known endemic richness. The results of other intertaxon diversity comparisons were highly variable, however. Based on our results, we suggest that protecting islands above a certain minimum threshold area may be the most efficient use of conservation resources. For example, using our island database, if the threshold were set at 10 km² and the smallest 10% of islands greater than this threshold were protected, 119 islands would be protected. The islands would range in size from 10 to 29 km² and would include 268 lesser known species endemic to a single island, along with 11 bird and mammal species endemic to a single island. Our results suggest that for islands of equivalent size, prioritization based on total or threatened bird and mammal diversity may also capture opportunities to protect lesser known species endemic to islands. Beneficios de los Taxa Poco Estudiados para la Conservación de la Diversidad de Aves y Mamíferos en Islas     

Patterns of Genetic Diversity and Its Loss in Mammalian Populations

Abstract:  Policy aimed at conserving biodiversity has focused on species diversity. Loss of genetic diversity, however, can affect population persistence, evolutionary potential, and individual fitness. Although mammals are a well-studied taxonomic group, a comprehensive assessment of mammalian genetic diversity based on modern molecular markers is lacking. We examined published microsatellite data from populations of 108 mammalian species to evaluate background patterns of genetic variability across taxa and body masses. We tested for loss of genetic diversity at the population level by asking whether populations that experienced demographic threats exhibited lower levels of genetic diversity. We also evaluated the effect of ascertainment bias (a reduction in variability when microsatellite primers are transferred across species) on our assessment of genetic diversity. Heterozygosity did not vary with body mass across species ranging in size from shrews to whales. Differences across taxonomic groupings were noted at the highest level, between populations of marsupial and placental mammals. We documented consistently lower heterozygosity, however, in populations that had experienced demographic threats across a wide range of mammalian species. We also documented a significant ( p = 0.01) reduction in heterozygosity as a result of ascertainment bias. Our results suggest that populations of both rare and common mammals are currently losing genetic diversity and that conservation efforts focused above the population level may fail to protect the breadth of persisting genetic diversity. Conservation policy makers may need to focus their efforts below the species level to stem further losses of genetic resources.     

Quantitative and Molecular Genetic Variation in Captive Cotton-Top Tamarins (Saguinus oedipus)

Most genetic surveys of captive and endangered populations are carried out with single gene characters bearing no direct relationship to life history or other features for which genetic variation needs to be maintained. Quantitative genetic estimates of heritable variation for life-history traits may be a more direct and appropriate measure of genetic variation for some conservation purposes. Furthermore, recent theoretical and empirical results indicate that genetic variation measured on these two levels may not be concordant. We analyzed heterozygosity at 41 allozyme loci and heritability for body weight in captive cotton-top tamarins ( Saguinus oedipus ) from the Marmoset Research Center of the Oak Ridge Associated Universities in order to compare these two levels of genetic variation. Cotton-top tamarins are a highly endangered species native to Colombia. Many animals currently reside in research facilities and zoological parks. A total of 106 animals were used in the isozyme survey, while data on 364 animals contributed to the quantitative genetic study of body weight. We found a very low average heterozygosity ( H = 1%) for this colony. Body weight was moderately and significantly heritable ( h ² = 35%). This heritability is within the normal range for natural animal populations. The finding of biologically significant levels of heritability in a population with abnormally low allozyme heterozygosity illustrates the point that low levels of allozyme heterozygosity should not be taken as an indication of overall lack of genetic variation in important quantitative characters such as life-history traits. Genetic variation required for adaptation of species to future environmental challenges can exist despite low levels of enzyme heterozygosity.