Demographic history shapes North American gray wolf genomic diversity and informs species' conservation.

Effective population size estimates are critical information needed for evolutionary predictions and conservation decisions. This is particularly true for species with social factors that restrict access to breeding or experience repeated fluctuations in population size across generations. We investigated the genomic estimates of effective population size along with diversity, subdivision, and inbreeding from 162,109 minimally filtered and 81,595 statistically neutral and unlinked SNPs genotyped in 437 grey wolf samples from North America collected between 1986 and 2021. We found genetic structure across North America, represented by three distinct demographic histories of western, central, and eastern regions of the continent. Further, grey wolves in the northern Rocky Mountains have lower genomic diversity than wolves of the western Great Lakes and have declined over time. Effective population size estimates revealed the historical signatures of continental efforts of predator extermination, despite a quarter century of recovery efforts. We are the first to provide molecular estimates of effective population size across distinct grey wolf populations in North America, which ranged between Ne ~ 275 and 3050 since early 1980s. We provide data that inform managers regarding the status and importance of effective population size estimates for grey wolf conservation, which are on average 5.2-9.3% of census estimates for this species. We show that while grey wolves fall above minimum effective population sizes needed to avoid extinction due to inbreeding depression in the short term, they are below sizes predicted to be necessary to avoid long-term risk of extinction.

Links between three chronic and age-related diseases, osteoarthritis, periodontitis, and osteoporosis, in a wild mammal (moose) population.

OBJECTIVE: Osteoarthritis, periodontitis and osteoporosis are chronic, age-related diseases which adversely impact millions of people worldwide. Because these diseases pose a major global public health challenge, there is an urgent need to better understand how these diseases are interrelated. Our objective was to document the age and sex-specific prevalence of each disease and assess interrelationships among the three diseases in a wild mammal (moose, Alces alces) population. METHODS: We examined the bones of moose dying from natural causes and recorded the severity of osteoarthritis (typically observed on the hip and lowest vertebrae), osteoporosis (osteoporotic lesions observed on the skull) and periodontitis (observed on maxilla and mandibles). RESULTS: Periodontitis was associated with a greater prevalence of both severe osteoarthritis and osteoporotic lesions in moose. We found no evidence to suggest that moose with osteoporotic lesions were more or less likely to exhibit signs of osteoarthritis or severe osteoarthritis. The prevalence of osteoarthritis, periodontitis and osteoporotic lesions was greater among males than for females. CONCLUSIONS: Our results were consistent with the hypothesis that bacterial pathogens causing periodontitis are a risk factor for osteoarthritis and osteoporosis. They are also consistent with the hypothesis that the inverse association between osteoarthritis and osteoporosis sometimes observed in humans may be influenced by shared risk factors, such as obesity, smoking or alcohol consumption, which are absent in moose. Together these results provide insights about three diseases which are expected to become more prevalent in the future and that cause substantial socio-economic burdens.

The difficulty of detecting inbreeding depression and its effect on conservation decisions.

Statistical inferences about inbreeding depression are often derived from analyses with low power and a high risk of failing to detect inbreeding depression. That risk is widely appreciated by scientists familiar with the relevant statistical and genetical theory, but may be overlooked and underappreciated by decision-makers. Consequently, there is value in demonstrating this risk using a real example. We use data from the wolf population on Isle Royale to demonstrate the difficulty of making reliable statistical inferences about inbreeding depression. This wolf population is known-by other methods-to have gone effectively extinct due to deleterious genetic processes associated with inbreeding. Beyond that demonstration, we use two case-studies-wolves on Isle Royale and vaquita (porpoises) from the Gulf of California, Mexico-to show how statistical inferences about inbreeding depression can affect conservation decisions. According to most decision theory, decisions depend importantly on: 1) probabilities that certain states exist (e.g. inbreeding depression is present) and 2) the utility assigned to various outcomes (e.g. the value of acting to mitigate inbreeding when it is present). The probabilities are provided by statistical inference; whereas utilities are almost entirely determined by normative values and judgements. Our analysis suggests that decisions to mitigate inbreeding depression are often driven more by utilities (normative values) than probabilities (statistical inferences). As such, advocates for mitigating inbreeding depression will benefit from better communicating to decision-makers the value of populations persisting and the extent to which decisions should depend on normative values.

The far-reaching effects of genetic process in a keystone predator species, grey wolves.

Although detrimental genetic processes are known to adversely affect the viability of populations, little is known about how detrimental genetic processes in a keystone species can affect the functioning of ecosystems. Here, we assessed how changes in the genetic characteristics of a keystone predator, grey wolves, affected the ecosystem of Isle Royale National Park over two decades. Changes in the genetic characteristic of the wolf population associated with a genetic rescue event, followed by high levels of inbreeding, led to a rise and then fall in predation rates on moose, the primary prey of wolves and dominant mammalian herbivore in this system. Those changes in predation rate led to large fluctuations in moose abundance, which in turn affected browse rates on balsam fir, the dominant forage for moose during winter and an important boreal forest species. Thus, forest dynamics can be traced back to changes in the genetic characteristics of a predator population.

Genomic Underpinnings of Population Persistence in Isle Royale Moose.

Island ecosystems provide natural laboratories to assess the impacts of isolation on population persistence. However, most studies of persistence have focused on a single species, without comparisons to other organisms they interact with in the ecosystem. The case study of moose and gray wolves on Isle Royale allows for a direct contrast of genetic variation in isolated populations that have experienced dramatically differing population trajectories over the past decade. Whereas the Isle Royale wolf population recently declined nearly to extinction due to severe inbreeding depression, the moose population has thrived and continues to persist, despite having low genetic diversity and being isolated for ∼120 years. Here, we examine the patterns of genomic variation underlying the continued persistence of the Isle Royale moose population. We document high levels of inbreeding in the population, roughly as high as the wolf population at the time of its decline. However, inbreeding in the moose population manifests in the form of intermediate-length runs of homozygosity suggestive of historical inbreeding and purging, contrasting with the long runs of homozygosity observed in the smaller wolf population. Using simulations, we confirm that substantial purging has likely occurred in the moose population. However, we also document notable increases in genetic load, which could eventually threaten population viability over the long term. Overall, our results demonstrate a complex relationship between inbreeding, genetic diversity, and population viability that highlights the use of genomic datasets and computational simulation tools for understanding the factors enabling persistence in isolated populations.

The role of governance in rewilding the United States to stem the biodiversity crisis.

A critical but underattended feature of the biodiversity crisis is the contraction of geographic range experienced by most studied terrestrial vertebrates. In the United States, the primary policy tool for mitigating the biodiversity crisis is a federal law, the Endangered Species Act (ESA). For the past two decades, the federal agencies that administer the ESA have interpreted the act in a manner that precludes treating this geographic element of the crisis. Therefore, the burden of mitigating the biodiversity crisis largely falls on wildlife agencies within state government, which are obligated to operate on behalf of the interests of their constituents. We present survey research indicating that most constituents expect state agencies to prioritize species restoration over other activities, including hunting. This prioritization holds even among self-identified hunters, which is significant because state agencies often take the provisioning of hunting opportunity as their top priority. By prioritizing rewilding efforts that restore native species throughout portions of their historic range, state agencies could unify hunting and nonhunting constituents while simultaneously stemming the biodiversity crisis.

Finding Purpose in the Conservation of Biodiversity by the Commingling of Science and Ethics.

Averting the biodiversity crisis requires closing a gap between how humans tend to behave, individually and collectively, and how we ought to behave-"ought to" in the sense of behaviors required to avert the biodiversity crisis. Closing that gap requires synthesizing insight from ethics with insights from social and behavioral sciences. This article contributes to that synthesis, which presents in several provocative hypotheses: (i) Lessening the biodiversity crisis requires promoting pro-conservation behavior among humans. Doing so requires better scientific understanding of how one's sense of purpose in life affects conservation-relevant behaviors. Psychology and virtue-focused ethics indicate that behavior is importantly influenced by one's purpose. However, conservation psychology has neglected inquiries on (a) the influence of one's purpose (both the content and strength of one's purpose) on conservation-related behaviors and (b) how to foster pro-conservation purposes; (ii) lessening the biodiversity crisis requires governance-the regulation of behavior by governments, markets or other organization through various means, including laws, norms, and power-to explicitly take conservation as one of its fundamental purposes and to do so across scales of human behaviors, from local communities to nations and corporations; (iii) lessening the biodiversity crisis requires intervention via governance to nudge human behavior in line with the purpose of conservation without undue infringement on other basic values. Aligning human behavior with conservation is inhibited by the underlying purpose of conservation being underspecified. Adequate specification of conservation's purpose will require additional interdisciplinary research involving insights from ethics, social and behavioral sciences, and conservation biology.

Territoriality drives preemptive habitat selection in recovering wolves: Implications for carnivore conservation.

According to the ideal-free distribution (IFD), individuals within a population are free to select habitats that maximize their chances of success. Assuming knowledge of habitat quality, the IFD predicts that average fitness will be approximately equal among individuals and between habitats, while density varies, implying that habitat selection will be density dependent. Populations are often assumed to follow an IFD, although this assumption is rarely tested with empirical data, and may be incorrect when territoriality indicates habitat selection tactics that deviate from the IFD (e.g. ideal-despotic distribution or ideal-preemptive distribution). When territoriality influences habitat selection, species' density will not directly reflect components of fitness such as reproductive success or survival. In such cases, assuming an IFD can lead to false conclusions about habitat quality. We tested theoretical models of density-dependent habitat selection on a species known to exhibit territorial behaviour in order to determine whether commonly applied habitat models are appropriate under these circumstances. We combined long-term radiotelemetry and census data from grey wolves Canis lupus in the Upper Peninsula of Michigan, USA to relate spatiotemporal variability in wolf density to underlying classifications of habitat within a hierarchical state-space modelling framework. We then iteratively applied isodar analysis to evaluate which distribution of habitat selection best described this recolonizing wolf population. The wolf population in our study expanded by >1,000% during our study (~50 to >600 individuals), and density-dependent habitat selection was most consistent with the ideal-preemptive distribution, as opposed to the ideal-free or ideal-despotic alternatives. Population density of terrestrial carnivores may not be positively correlated with the fitness value of their habitats, and density-dependent habitat selection patterns may help to explain complex predator-prey dynamics and cascading indirect effects. Source-sink population dynamics appear likely when species exhibit rapid growth and occupy interspersed habitats of contrasting quality. These conditions are likely and have implications for large carnivores in many systems, such as areas in North America and Europe where large predator species are currently recolonizing their former ranges.

Tooth fracture frequency in gray wolves reflects prey availability.

Exceptionally high rates of tooth fracture in large Pleistocene carnivorans imply intensified interspecific competition, given that tooth fracture rises with increased bone consumption, a behavior that likely occurs when prey are difficult to acquire. To assess the link between prey availability and dental attrition, we documented dental fracture rates over decades among three well-studied populations of extant gray wolves that differed in prey:predator ratio and levels of carcass utilization. When prey:predator ratios declined, kills were more fully consumed, and rates of tooth fracture more than doubled. This supports tooth fracture frequency as a relative measure of the difficulty of acquiring prey, and reveals a rapid response to diminished food levels in large carnivores despite risks of infection and reduced fitness due to dental injuries. More broadly, large carnivore tooth fracture frequency likely reflects energetic stress, an aspect of predator success that is challenging to quantify in wild populations.

Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction.

The observation that small isolated populations often suffer reduced fitness from inbreeding depression has guided conservation theory and practice for decades. However, investigating the genome-wide dynamics associated with inbreeding depression in natural populations is only now feasible with relatively inexpensive sequencing technology and annotated reference genomes. To characterize the genome-wide effects of intense inbreeding and isolation, we performed whole-genome sequencing and morphological analysis of an iconic inbred population, the gray wolves (Canis lupus) of Isle Royale. Through population genetic simulations and comparison with wolf genomes from a variety of demographic histories, we find evidence that severe inbreeding depression in this population is due to increased homozygosity of strongly deleterious recessive mutations. Our results have particular relevance in light of the recent translocation of wolves from the mainland to Isle Royale, as well as broader implications for management of genetic variation in the fragmented landscape of the modern world.

Negative frequency-dependent foraging behaviour in a generalist herbivore (Alces alces) and its stabilizing influence on food web dynamics.

Resource selection is widely appreciated to be context-dependent and shaped by both biological and abiotic factors. However, few studies have empirically assessed the extent to which selective foraging behaviour is dynamic and varies in response to environmental conditions for free-ranging animal populations. Here, we assessed the extent that forage selection fluctuated in response to different environmental conditions for a free-ranging herbivore, moose (Alces alces), in Isle Royale National Park, over a 10-year period. More precisely, we assessed how moose selection for coniferous versus deciduous forage in winter varied between geographic regions and in relation to (a) the relative frequency of forage types in the environment (e.g. frequency-dependent foraging behaviour), (b) moose abundance, (c) predation rate (by grey wolves) and (d) snow depth. These factors are potentially important for their influence on the energetics of foraging. We also built a series of food-chain models to assess the influence of dynamic foraging strategies on the stability of food webs. Our analysis indicates that moose exhibited negative frequency dependence, by selectively exploiting rare resources. Frequency-dependent foraging was further mediated by density-dependent processes, which are likely to be predation, moose abundance or some combination of both. In particular, frequency dependence was weaker in years when predation risk was high (i.e. when the ratio of moose to wolves was relatively low). Selection for conifers was also slightly weaker during deep snow years. The food-chain analysis indicates that the type of frequency-dependent foraging strategy exhibited by herbivores had important consequences for the stability of ecological communities. In particular, the dynamic foraging strategy that we observed in the empirical analysis (i.e. negative frequency dependence being mediated by density-dependent processes) was associated with more stable food web dynamics compared to fixed foraging strategies. The results of this study indicated that forage selection is a complex ecological process, varying in response to both biological (predation and moose density) and abiotic factors (snow depth) and over relatively small spatial scales (between regions). This study also provides a useful framework for assessing the influence of other aspects of foraging behaviour on the stability of food web dynamics.

The Ethics of Human⁻Animal Relationships and Public Discourse: A Case Study of Lions Bred for Their Bones.

Conservation and natural resource management are increasingly attending the ethical elements of public decisions. Ethical considerations are challenging, in part, because they typically require accounting for the moral consideration of various human and nonhuman forms of life, whose interests sometimes conflict (or seem to conflict). A valuable tool for such evaluations is the formal analysis of ethical arguments. An ethical argument is a collection of premises, logically interrelated, to yield a conclusion that can be expressed in the form, "We ought to…" According to the rules of logic, a conclusion is supported by an argument if all its premises are true or appropriate and when it contains no mistaken inferences. We showed how the formal analysis of ethical arguments can be used to engage stakeholders and decision-makers in decision-making processes. We summarised the method with ten specific guidelines that would be applicable to any case. We illustrated the technique using a case study focused on captive-bred lions, the skeletons of which form part of an international trade to supply traditional medicine markets in Southeast Asia with felid bones. As a matter of public policy, the practice is a complicated nexus of concerns for entrepreneurial freedom, wildlife conservation, and the fair treatment of animals.

Does persistent snowpack inhibit degradation of fecal stress indicators?

Physiological stress in wildlife can be a useful indicator of a population's response to environmental factors. By using non-invasive endocrinological techniques, such as fecal sampling, potential confounding factors associated with the stress of capture can be avoided. A potential drawback of fecal sampling, however, is degradation of samples which may produce aberrant measurements of fecal glucocorticoid metabolites. In vertebrates, glucocorticoids, such as corticosterone, become elevated in response to stress. We sought to gauge the reliability of measurement of fecal glucocorticoid metabolites from white-tailed deer (Odocoileus virginianus) fecal samples exposed to a temperate winter with substantial snow cover and cold temperatures for up to 90 days, by repeatedly subsampling fecal samples every 10 days and performing a corticosterone enzyme-linked immunosorbent assay (ELISA). Measurements of fecal glucocorticoid metabolites at 10 days were consistent with initial measurements, after which (20 days) they became aberrant following a period of thawing. Consequently, glucocorticoid metabolite levels in feces appear to remain stable under ambient conditions if temperatures remain below freezing at least for 10 days. While it's possible that samples may remain useful beyond this time frame based on previous laboratory studies of samples stored in a freezer, further work is needed to determine how samples weather in situ under extreme cold (e.g. Arctic) or periods of partial thawing.

Climate warming is associated with smaller body size and shorter lifespans in moose near their southern range limit.

Despite the importance of body size for individual fitness, population dynamics and community dynamics, the influence of climate change on growth and body size is inadequately understood, particularly for long-lived vertebrates. Although temporal trends in body size have been documented, it remains unclear whether these changes represent the adverse impact of climate change (environmental stress constraining phenotypes) or its mitigation (via phenotypic plasticity or evolution). Concerns have also been raised about whether climate change is indeed the causal agent of these phenotypic shifts, given the length of time-series analysed and that studies often do not evaluate - and thereby sufficiently rule out - other potential causes. Here, we evaluate evidence for climate-related changes in adult body size (indexed by skull size) over a 4-decade period for a population of moose (Alces alces) near the southern limit of their range whilst also considering changes in density, predation, and human activities. In particular, we document: (i) a trend of increasing winter temperatures and concurrent decline in skull size (decline of 19% for males and 13% for females) and (ii) evidence of a negative relationship between skull size and winter temperatures during the first year of life. These patterns could be plausibly interpreted as an adaptive phenotypic response to climate warming given that latitudinal/temperature clines are often accepted as evidence of adaptation to local climate. However, we also observed: (iii) that moose with smaller skulls had shorter lifespans, (iv) a reduction in lifespan over the 4-decade study period, and (v) a negative relationship between lifespan and winter temperatures during the first year of life. Those observations indicate that this phenotypic change is not an adaptive response to climate change. However, this decline in lifespan was not accompanied by an obvious change in population dynamics, suggesting that climate change may affect population dynamics and life-histories differently.

Genomic Variation of Inbreeding and Ancestry in the Remaining Two Isle Royale Wolves.

Inbreeding, relatedness, and ancestry have traditionally been estimated with pedigree information, however, molecular genomic data can provide more detailed examination of these properties. For example, pedigree information provides estimation of the expected value of these measures but molecular genomic data can estimate the realized values of these measures in individuals. Here, we generate the theoretical distribution of inbreeding, relatedness, and ancestry for the individuals in the pedigree of the Isle Royale wolves, the first examination of such variation in a wild population with a known pedigree. We use the 38 autosomes of the dog genome and their estimated map lengths in our genomic analysis. Although it is known that the remaining wolves are highly inbred, closely related, and descend from only 3 ancestors, our analyses suggest that there is significant variation in the realized inbreeding and relatedness around pedigree expectations. For example, the expected inbreeding in a hypothetical offspring from the 2 remaining wolves is 0.438 but the realized 95% genomic confidence interval is from 0.311 to 0.565. For individual chromosomes, a substantial proportion of the whole chromosomes are completely identical by descent. This examination provides a background to use when analyzing molecular genomic data for individual levels of inbreeding, relatedness, and ancestry. The level of variation in these measures is a function of the time to the common ancestor(s), the number of chromosomes, and the rate of recombination. In the Isle Royale wolf population, the few generations to a common ancestor results in the high variance in genomic inbreeding.

Interannual variability: a crucial component of space use at the territory level.

Interannual variability in space use and how that variation is influenced by density-dependent and density-independent factors are important processes in population ecology. Nevertheless, interannual variability has been neglected by the majority of space use studies. We assessed that variation for wolves living in 15 different packs within Yellowstone National Park during a 13-year period (1996-2008). We estimated utilization distributions to quantify the intensity of space use within each pack's territory each year in summer and winter. Then, we used the volume of intersection index (VI) to quantify the extent to which space use varied from year to year. This index accounts for both the area of overlap and differences in the intensity of use throughout a territory and ranges between 0 and 1. The mean VI index was 0.49, and varied considerably, with approximately 20% of observations (n = 230) being <0.3 or >0.7. In summer, 42% of the variation was attributable to differences between packs. These differences can be attributable to learned behaviors and had never been thought to have such an influence on space use. In winter, 34% of the variation in overlap between years was attributable to interannual differences in precipitation and pack size. This result reveals the strong influence of climate on predator space use and underlies the importance of understanding how climatic factors are going to affect predator populations in the occurrence of climate change. We did not find any significant association between overlap and variables representing density-dependent processes (elk and wolf densities) or intraspecific competition (ratio of wolves to elk). This last result poses a challenge to the classic view of predator-prey systems. On a small spatial scale, predator space use may be driven by factors other than prey distribution.

Evaluating whether nature's intrinsic value is an axiom of or anathema to conservation.

That at least some aspects of nature possess intrinsic value is considered by some an axiom of conservation. Others consider nature's intrinsic value superfluous or anathema. This range of views among mainstream conservation professionals potentially threatens the foundation of conservation. One challenge in resolving this disparity is that disparaging portrayals of nature's intrinsic value appear rooted in misconceptions and unfounded presumptions about what it means to acknowledge nature's intrinsic value. That acknowledgment has been characterized as vacuous, misanthropic, of little practical consequence to conservation, adequately accommodated by economic valuation, and not widely accepted in society. We reviewed the philosophical basis for nature's intrinsic value and the implications for acknowledging that value. Our analysis is rooted to the notion that when something possesses intrinsic value it deserves to be treated with respect for what it is, with concern for its welfare or in a just manner. From this basis, one can only conclude that nature's intrinsic value is not a vacuous concept or adequately accommodated by economic valuation. Acknowledging nature's intrinsic value is not misanthropic because concern for nature's welfare (aside from its influence on human welfare) does not in any way preclude also being concerned for human welfare. The practical import of acknowledging nature's intrinsic value rises from recognizing all the objects of conservation concern (e.g., many endangered species) that offer little benefit to human welfare. Sociological and cultural evidence indicates the belief that at least some elements of nature possess intrinsic value is widespread in society. Our reasoning suggests the appropriateness of rejecting the assertion that nature's intrinsic value is anathema to conservation and accepting its role as an axiom.