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.

Density-dependent habitat selection alters drivers of population distribution in northern Yellowstone elk.

Although it is well established that density dependence drives changes in organismal abundance over time, relatively little is known about how density dependence affects variation in abundance over space. We tested the hypothesis that spatial trade-offs between food and safety can change the drivers of population distribution, caused by opposing patterns of density-dependent habitat selection (DDHS) that are predicted by the multidimensional ideal free distribution. We addressed this using winter aerial survey data of northern Yellowstone elk (Cervus canadensis) spanning four decades. Supporting our hypothesis, we found positive DDHS for food (herbaceous biomass) and negative DDHS for safety (openness and roughness), such that the primary driver of habitat selection switched from food to safety as elk density decreased from 9.3 to 2.0 elk/km2 . Our results demonstrate how population density can drive landscape-level shifts in population distribution, confounding habitat selection inference and prediction and potentially affecting community-level interactions.

Patterns of reproduction and autozygosity distinguish the breeding from non-breeding gray wolves of Yellowstone National Park.

For species of management concern, accurate estimates of inbreeding and associated consequences on reproduction are crucial for predicting their future viability. However, few studies have partitioned this aspect of genetic viability with respect to reproduction in a group-living social mammal. We investigated the contributions of foundation stock lineages, putative fitness consequences of inbreeding, and genetic diversity of the breeding versus non-reproductive segment of the Yellowstone National Park gray wolf population. Our dataset spans 25 years and seven generations since reintroduction, encompassing 152 nuclear families and 329 litters. We found over 87% of the pedigree foundation genomes persisted and report influxes of allelic diversity from two translocated wolves from a divergent source in Montana. As expected for group-living species, mean kinship significantly increased over time but with minimal loss of observed heterozygosity. Strikingly, the reproductive portion of the population carried a significantly lower genome-wide inbreeding coefficients, autozygosity, and more rapid decay for linkage disequilibrium relative to the non-breeding population. Breeding wolves had significantly longer lifespans and lower inbreeding coefficients than non-breeding wolves. Our model revealed that the number of litters was negatively significantly associated with heterozygosity (R=-0.11). Our findings highlight genetic contributions to fitness, and the importance of the reproductively active individuals in a population to counteract loss of genetic variation in a wild, free-ranging social carnivore. It is crucial for managers to mitigate factors that significantly reduce effective population size and genetic connectivity, which supports the dispersion of genetic variation that aids in rapid evolutionary responses to environmental challenges.

Examination of the interaction between age-specific predation and chronic disease in the Greater Yellowstone Ecosystem.

Predators may create healthier prey populations by selectively removing diseased individuals. Predators typically prefer some ages of prey over others, which may, or may not, align with those prey ages that are most likely to be diseased. The interaction of age-specific infection and predation has not been previously explored and likely has sizable effects on disease dynamics. We hypothesize that predator cleansing effects will be greater when the disease and predation occur in the same prey age groups. We examine the predator cleansing effect using a model where both vulnerability to predators and pathogen prevalence vary with age. We tailor this model to chronic wasting disease (CWD) in mule deer and elk populations in the Greater Yellowstone Ecosystem, with empirical data from Yellowstone grey wolves and cougars. Model results suggest that under moderate, yet realistic, predation pressure from cougars and wolves independently, predators may decrease CWD outbreak size substantially and delay the accumulation of symptomatic deer and elk. The magnitude of this effect is driven by the ability of predators to selectively remove late-stage CWD infections that are likely the most responsible for transmission, but this may not be the age class they typically select. Thus, predators that select for infected young adults over uninfected juveniles have a stronger cleansing effect, and these effects are strengthened when transmission rates increase with increasing prey morbidity. There are also trade-offs from a management perspective-that is, increasing predator kill rates can result in opposing forces on prey abundance and CWD prevalence. Our modelling exploration shows that predators have the potential to reduce prevalence in prey populations when prey age and disease severity are considered, yet the strength of this effect is influenced by predators' selection for demography or body condition. Current CWD management focuses on increasing cervid hunting as the primary management tool, and our results suggest predators may also be a useful tool under certain conditions, but not necessarily without additional impacts on host abundance and demography. Protected areas with predator populations will play a large role in informing the debate over predator impacts on disease.

Group density, disease, and season shape territory size and overlap of social carnivores.

The spatial organization of a population can influence the spread of information, behaviour and pathogens. Group territory size and territory overlap and components of spatial organization, provide key information as these metrics may be indicators of habitat quality, resource dispersion, contact rates and environmental risk (e.g. indirectly transmitted pathogens). Furthermore, sociality and behaviour can also shape space use, and subsequently, how space use and habitat quality together impact demography. Our study aims to identify factors shaping the spatial organization of wildlife populations and assess the impact of epizootics on space use. We further aim to explore the mechanisms by which disease perturbations could cause changes in spatial organization. Here we assessed the seasonal spatial organization of Serengeti lions and Yellowstone wolves at the group level. We use network analysis to describe spatial organization and connectivity of social groups. We then examine the factors predicting mean territory size and mean territory overlap for each population using generalized additive models. We demonstrate that lions and wolves were similar in that group-level factors, such as number of groups and shaped spatial organization more than population-level factors, such as population density. Factors shaping territory size were slightly different than factors shaping territory overlap; for example, wolf pack size was an important predictor of territory overlap, but not territory size. Lion spatial networks were more highly connected, while wolf spatial networks varied seasonally. We found that resource dispersion may be more important for driving territory size and overlap for wolves than for lions. Additionally, canine distemper epizootics may have altered lion spatial organization, highlighting the importance of including infectious disease epizootics in studies of behavioural and movement ecology. We provide insight about when we might expect to observe the impacts of resource dispersion, disease perturbations, and other ecological factors on spatial organization. Our work highlights the importance of monitoring and managing social carnivore populations at the group level. Future research should elucidate the complex relationships between demographics, social and spatial structure, abiotic and biotic conditions and pathogen infections.

K Locus Effects in Gray Wolves: Experimental Assessment of TLR3 Signaling and the Gene Expression Response to Canine Distemper Virus.

In North American gray wolves, black coat color is dominantly inherited via a 3 base pair coding deletion in the canine beta defensin 3 (CBD103) gene. This 3 base pair deletion, called the KB allele, was introduced through hybridization with dogs and subsequently underwent a selective sweep that increased its frequency in wild wolves. Despite apparent positive selection, KBB wolves have lower fitness than wolves with the KyB genotype, even though the 2 genotypes show no observable differences in black coat color. Thus, the KB allele is thought to have pleiotropic effects on as-yet unknown phenotypes. Given the role of skin-expressed CBD103 in innate immunity, we hypothesized that the KB allele influences the keratinocyte gene expression response to TLR3 pathway stimulation and/or infection by canine distemper virus (CDV). To test this hypothesis, we developed a panel of primary epidermal keratinocyte cell cultures from 24 wild North American gray wolves of both Kyy and KyB genotypes. In addition, we generated an immortalized Kyy line and used CRISPR/Cas9 editing to produce a KyB line on the same genetic background. We assessed the transcriptome-wide responses of wolf keratinocytes to the TLR3 agonist polyinosinic:polycytidylic acid (polyI:C), and to live CDV. K locus genotype did not predict the transcriptional response to either challenge, suggesting that variation in the gene expression response does not explain pleiotropic effects of the KB allele on fitness. This study supports the feasibility of using cell culture methods to investigate the phenotypic effects of naturally occurring genetic variation in wild mammals.

De Novo Mutation Rate Estimation in Wolves of Known Pedigree.

Knowledge of mutation rates is crucial for calibrating population genetics models of demographic history in units of years. However, mutation rates remain challenging to estimate because of the need to identify extremely rare events. We estimated the nuclear mutation rate in wolves by identifying de novo mutations in a pedigree of seven wolves. Putative de novo mutations were discovered by whole-genome sequencing and were verified by Sanger sequencing of parents and offspring. Using stringent filters and an estimate of the false negative rate in the remaining observable genome, we obtain an estimate of ∼4.5 × 10-9 per base pair per generation and provide conservative bounds between 2.6 × 10-9 and 7.1 × 10-9. Although our estimate is consistent with recent mutation rate estimates from ancient DNA (4.0 × 10-9 and 3.0-4.5 × 10-9), it suggests a wider possible range. We also examined the consequences of our rate and the accompanying interval for dating several critical events in canid demographic history. For example, applying our full range of rates to coalescent models of dog and wolf demographic history implies a wide set of possible divergence times between the ancestral populations of dogs and extant Eurasian wolves (16,000-64,000 years ago) although our point estimate indicates a date between 25,000 and 33,000 years ago. Aside from one study in mice, ours provides the only direct mammalian mutation rate outside of primates and is likely to be vital to future investigations of mutation rate evolution.

Heritability of interpack aggression in a wild pedigreed population of North American grey wolves.

Aggression is a quantitative trait deeply entwined with individual fitness. Mapping the genomic architecture underlying such traits is complicated by complex inheritance patterns, social structure, pedigree information and gene pleiotropy. Here, we leveraged the pedigree of a reintroduced population of grey wolves (Canis lupus) in Yellowstone National Park, Wyoming, USA, to examine the heritability of and the genetic variation associated with aggression. Since their reintroduction, many ecological and behavioural aspects have been documented, providing unmatched records of aggressive behaviour across multiple generations of a wild population of wolves. Using a linear mixed model, a robust genetic relationship matrix, 12,288 single nucleotide polymorphisms (SNPs) and 111 wolves, we estimated the SNP-based heritability of aggression to be 37% and an additional 14% of the phenotypic variation explained by shared environmental exposures. We identified 598 SNP genotypes from 425 grey wolves to resolve a consensus pedigree that was included in a heritability analysis of 141 individuals with SNP genotype, metadata and aggression data. The pedigree-based heritability estimate for aggression is 14%, and an additional 16% of the phenotypic variation was explained by shared environmental exposures. We find strong effects of breeding status and relative pack size on aggression. Through an integrative approach, these results provide a framework for understanding the genetic architecture of a complex trait that influences individual fitness, with linkages to reproduction, in a social carnivore. Along with a few other studies, we show here the incredible utility of a pedigreed natural population for dissecting a complex, fitness-related behavioural trait.

How climate impacts the composition of wolf-killed elk in northern Yellowstone National Park.

While the functional response of predators is commonly measured, recent work has revealed that the age and sex composition of prey killed is often a better predictor of prey population dynamics because the reproductive value of adult females is usually higher than that of males or juveniles. Climate is often an important mediating factor in determining the composition of predator kills, but we currently lack a mechanistic understanding of how the multiple facets of climate interact with prey abundance and demography to influence the composition of predator kills. Over 20 winters, we monitored 17 wolf packs in Yellowstone National Park and recorded the sex, age and nutritional condition of kills of their dominant prey-elk-in both early and late winter periods when elk are in relatively good and relatively poor condition, respectively. Nutritional condition (as indicated by per cent marrow fat) of wolf-killed elk varied markedly with summer plant productivity, snow water equivalent (SWE) and winter period. Moreover, marrow was poorer for wolf-killed bulls and especially for calves than it was for cows. Wolf prey composition was influenced by a complex set of climatic and endogenous variables. In early winter, poor plant growth in either year t or t - 1, or relatively low elk abundance, increased the odds of wolves killing bulls relative to cows. Calves were most likely to get killed when elk abundance was high and when the forage productivity they experienced in utero was poor. In late winter, low SWE and a relatively large elk population increased the odds of wolves killing calves relative to cows, whereas low SWE and poor vegetation productivity 1 year prior together increased the likelihood of wolves killing a bull instead of a cow. Since climate has a strong influence on whether wolves prey on cows (who, depending on their age, are the key reproductive components of the population) or lower reproductive value of calves and bulls, our results suggest that climate can drive wolf predation to be more or less additive from year to year.

Weak spatiotemporal response of prey to predation risk in a freely interacting system.

The extent to which prey space use actively minimizes predation risk continues to ignite controversy. Methodological reasons that have hindered consensus include inconsistent measurements of predation risk, biased spatiotemporal scales at which responses are measured and lack of robust null expectations. We addressed all three challenges in a comprehensive analysis of the spatiotemporal responses of adult female elk (Cervus elaphus) to the risk of predation by wolves (Canis lupus) during winter in northern Yellowstone, USA. We quantified spatial overlap between the winter home ranges of GPS-collared elk and three measures of predation risk: the intensity of wolf space use, the distribution of wolf-killed elk and vegetation openness. We also assessed whether elk varied their use of areas characterized by more or less predation risk across hours of the day, and estimated encounter rates between simultaneous elk and wolf pack trajectories. We determined whether observed values were significantly lower than expected if elk movements were random with reference to predation risk using a null model approach. Although a small proportion of elk did show a tendency to minimize use of open vegetation at specific times of the day, overall we highlight a notable absence of spatiotemporal response by female elk to the risk of predation posed by wolves in northern Yellowstone. Our results suggest that predator-prey interactions may not always result in strong spatiotemporal patterns of avoidance.

Do prey select for vacant hunting domains to minimize a multi-predator threat?

Many ecosystems contain sympatric predator species that hunt in different places and times. We tested whether this provides vacant hunting domains, places and times where and when predators are least active, that prey use to minimize threats from multiple predators simultaneously. We measured how northern Yellowstone elk (Cervus elaphus) responded to wolves (Canis lupus) and cougars (Puma concolor), and found that elk selected for areas outside the high-risk domains of both predators consistent with the vacant domain hypothesis. This enabled elk to avoid one predator without necessarily increasing its exposure to the other. Our results demonstrate how the diel cycle can serve as a key axis of the predator hunting domain that prey exploit to manage predation risk from multiple sources. We argue that a multi-predator, spatiotemporal framework is vital to understand the causes and consequences of prey spatial response to predation risk in environments with more than one predator.

Natural Selection and Origin of a Melanistic Allele in North American Gray Wolves.

Pigmentation is often used to understand how natural selection affects genetic variation in wild populations since it can have a simple genetic basis, and can affect a variety of fitness-related traits (e.g., camouflage, thermoregulation, and sexual display). In gray wolves, the K locus, a ß-defensin gene, causes black coat color via a dominantly inherited KB allele. The allele is derived from dog-wolf hybridization and is at high frequency in North American wolf populations. We designed a DNA capture array to probe the geographic origin, age, and number of introgression events of the KB allele in a panel of 331 wolves and 20 dogs. We found low diversity in KB, but not ancestral ky, wolf haplotypes consistent with a selective sweep of the black haplotype across North America. Further, North American wolf KB haplotypes are monophyletic, suggesting that a single adaptive introgression from dogs to wolves most likely occurred in the Northwest Territories or Yukon. We use a new analytical approach to date the origin of the KB allele in Yukon wolves to between 1,598 and 7,248 years ago, suggesting that introgression with early Native American dogs was the source. Using population genetic simulations, we show that the K locus is undergoing natural selection in four wolf populations. We find evidence for balancing selection, specifically in Yellowstone wolves, which could be a result of selection for enhanced immunity in response to distemper. With these data, we demonstrate how the spread of an adaptive variant may have occurred across a species' geographic range.

Pervasive Effects of Aging on Gene Expression in Wild Wolves.

Gene expression levels change as an individual ages and responds to environmental conditions. With the exception of humans, such patterns have principally been studied under controlled conditions, overlooking the array of developmental and environmental influences that organisms encounter under conditions in which natural selection operates. We used high-throughput RNA sequencing (RNA-Seq) of whole blood to assess the relative impacts of social status, age, disease, and sex on gene expression levels in a natural population of gray wolves (Canis lupus). Our findings suggest that age is broadly associated with gene expression levels, whereas other examined factors have minimal effects on gene expression patterns. Further, our results reveal evolutionarily conserved signatures of senescence, such as immunosenescence and metabolic aging, between wolves and humans despite major differences in life history and environment. The effects of aging on gene expression levels in wolves exhibit conservation with humans, but the more rapid expression differences observed in aging wolves is evolutionarily appropriate given the species' high level of extrinsic mortality due to intraspecific aggression. Some expression changes that occur with age can facilitate physical age-related changes that may enhance fitness in older wolves. However, the expression of these ancestral patterns of aging in descendant modern dogs living in highly modified domestic environments may be maladaptive and cause disease. This work provides evolutionary insight into aging patterns observed in domestic dogs and demonstrates the applicability of studying natural populations to investigate the mechanisms of aging.

Competition between apex predators? Brown bears decrease wolf kill rate on two continents.

Trophic interactions are a fundamental topic in ecology, but we know little about how competition between apex predators affects predation, the mechanism driving top-down forcing in ecosystems. We used long-term datasets from Scandinavia (Europe) and Yellowstone National Park (North America) to evaluate how grey wolf (Canis lupus) kill rate was affected by a sympatric apex predator, the brown bear (Ursus arctos). We used kill interval (i.e. the number of days between consecutive ungulate kills) as a proxy of kill rate. Although brown bears can monopolize wolf kills, we found no support in either study system for the common assumption that they cause wolves to kill more often. On the contrary, our results showed the opposite effect. In Scandinavia, wolf packs sympatric with brown bears killed less often than allopatric packs during both spring (after bear den emergence) and summer. Similarly, the presence of bears at wolf-killed ungulates was associated with wolves killing less often during summer in Yellowstone. The consistency in results between the two systems suggests that brown bear presence actually reduces wolf kill rate. Our results suggest that the influence of predation on lower trophic levels may depend on the composition of predator communities.

The concerted impact of domestication and transposon insertions on methylation patterns between dogs and grey wolves.

The process of domestication can exert intense trait-targeted selection on genes and regulatory regions. Specifically, rapid shifts in the structure and sequence of genomic regulatory elements could provide an explanation for the extensive, and sometimes extreme, variation in phenotypic traits observed in domesticated species. Here, we explored methylation differences from >24 000 cytosines distributed across the genomes of the domesticated dog (Canis familiaris) and the grey wolf (Canis lupus). PCA and model-based cluster analyses identified two primary groups, domestic vs. wild canids. A scan for significantly differentially methylated sites (DMSs) revealed species-specific patterns at 68 sites after correcting for cell heterogeneity, with weak yet significant hypermethylation typical of purebred dogs when compared to wolves (59% and 58%, P < 0.05, respectively). Additionally, methylation patterns at eight genes significantly deviated from neutrality, with similar trends of hypermethylation in purebred dogs. The majority (>66%) of differentially methylated regions contained or were associated with repetitive elements, indicative of a genotype-mediated trend. However, DMSs were also often linked to functionally relevant genes (e.g. neurotransmitters). Finally, we utilized known genealogical relationships among Yellowstone wolves to survey transmission stability of methylation marks, from which we found a substantial fraction that demonstrated high heritability (both H(2) and h(2 ) > 0.99). These analyses provide a unique epigenetic insight into the molecular consequences of recent selection and radiation of our most ancient domesticated companion, the dog. These findings suggest selection has acted on methylation patterns, providing a new genomic perspective on phenotypic diversification in domesticated species.

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.

Density-dependent intraspecific aggression regulates survival in northern Yellowstone wolves (Canis lupus).

Understanding the population dynamics of top-predators is essential to assess their impact on ecosystems and to guide their management. Key to this understanding is identifying the mechanisms regulating vital rates. Determining the influence of density on survival is necessary to understand the extent to which human-caused mortality is compensatory or additive. In wolves (Canis lupus), empirical evidence for density-dependent survival is lacking. Dispersal is considered the principal way in which wolves adjust their numbers to prey supply or compensate for human exploitation. However, studies to date have primarily focused on exploited wolf populations, in which density-dependent mechanisms are likely weak due to artificially low wolf densities. Using 13 years of data on 280 collared wolves in Yellowstone National Park, we assessed the effect of wolf density, prey abundance and population structure, as well as winter severity, on age-specific survival in two areas (prey-rich vs. prey-poor) of the national park. We further analysed cause-specific mortality and explored the factors driving intraspecific aggression in the prey-rich northern area of the park. Overall, survival rates decreased during the study. In northern Yellowstone, density dependence regulated adult survival through an increase in intraspecific aggression, independent of prey availability. In the interior of the park, adult survival was less variable and density-independent, despite reduced prey availability. There was no effect of prey population structure in northern Yellowstone, or of winter severity in either area. Survival was similar among yearlings and adults, but lower for adults older than 6 years. Our results indicate that density-dependent intraspecific aggression is a major driver of adult wolf survival in northern Yellowstone, suggesting intrinsic density-dependent mechanisms have the potential to regulate wolf populations at high ungulate densities. When low prey availability or high removal rates maintain wolves at lower densities, limited inter-pack interactions may prevent density-dependent survival, consistent with our findings in the interior of the park.

Heterozygote Advantage in a Finite Population: Black Color in Wolves.

There is a striking color polymorphism for wolves in the Yellowstone National Park where approximately half the wolves are black. The genetic basis for this polymorphism is known, and fitnesses of the genotypes are estimated. These estimates suggest that there is strong heterozygote advantage but substantial asymmetry in the fitness differences of the 2 homozygotes. Theoretically, such fitnesses in a finite population are thought to reduce genetic variation at least as fast as if there were no selection at all. Because the color polymorphism has remained at about the same frequency for 17 years, about 4 generations, we investigated whether this was consistent with the theoretical predictions. Counter to this general expectation of loss, given the initial frequency of black wolves, the theoretical expectation in this case was found to be that the frequency would only decline slowly over time. For example, if the effective population size is 20, then the expected black allele frequency after 4 generations would be 0.191, somewhat less than the observed value of 0.237. However, nearly 30% of the time the expected frequency is 0.25 or greater, consistent with the contemporary observed frequency. In other words and in contrast to general theoretical predictions, because of the short period of time in evolutionary terms and the relatively weak selection at low frequencies, the observed variation and the predicted theoretical variation are not inconsistent.

Investigating tritrophic interactions using bioenergetic demographic models.

A central debate in ecology has been the long-running discussion on the role of apex predators in affecting the abundance and dynamics of their prey. In terrestrial systems, research has primarily relied on correlational approaches, due to the challenge of implementing robust experiments with replication and appropriate controls. A consequence of this is that we largely suffer from a lack of mechanistic understanding of the population dynamics of interacting species, which can be surprisingly complex. Mechanistic models offer an opportunity to examine the causes and consequences of some of this complexity. We present a bioenergetic mechanistic model of a tritrophic system where the primary vegetation resource follows a seasonal growth function, and the herbivore and carnivore species are modeled using two integral projection models (IPMs) with body mass as the phenotypic trait. Within each IPM, the demographic functions are structured according to bioenergetic principles, describing how animals acquire and transform resources into body mass, energy reserves, and breeding potential. We parameterize this model to reproduce the population dynamics of grass, elk, and wolves in northern Yellowstone National Park (USA) and investigate the impact of wolf reintroduction on the system. Our model generated predictions that closely matched the observed population sizes of elk and wolf in Yellowstone prior to and following wolf reintroduction. The introduction of wolves into our basal grass-elk bioenergetic model resulted in a population of 99 wolves and a reduction in elk numbers by 61% (from 14,948 to 5823) at equilibrium. In turn, vegetation biomass increased by approximately 25% in the growing season and more than threefold in the nongrowing season. The addition of wolves to the model caused the elk population to switch from being food-limited to being predator-limited and had a stabilizing effect on elk numbers across different years. Wolf predation also led to a shift in the phenotypic composition of the elk population via a small increase in elk average body mass. Our model represents a novel approach to the study of predator-prey interactions, and demonstrates that explicitly considering and linking bioenergetics, population demography and body mass phenotypes can provide novel insights into the mechanisms behind complex ecosystem processes.

From wolves to humans: oral microbiome resistance to transfer across mammalian hosts.

The mammalian mouth is colonized by complex microbial communities, adapted to specific niches, and in homeostasis with the host. Individual microbes interact metabolically and rely primarily on nutrients provided by the host, with which they have potentially co-evolved along the mammalian lineages. The oral environment is similar across mammals, but the diversity, specificity, and evolution of community structure in related or interacting mammals are little understood. Here, we compared the oral microbiomes of dogs with those of wild wolves and humans. In dogs, we found an increased microbial diversity relative to wolves, possibly related to the transition to omnivorous nutrition following domestication. This includes a larger diversity of Patescibacteria than previously reported in any other oral microbiota. The oral microbes are most distinct at bacterial species or strain levels, with few if any shared between humans and canids, while the close evolutionary relationship between wolves and dogs is reflected by numerous shared taxa. More taxa are shared at higher taxonomic levels including with humans, supporting their more ancestral common mammalian colonization followed by diversification. Phylogenies of selected oral bacterial lineages do not support stable human-dog microbial transfers but suggest diversification along mammalian lineages (apes and canids). Therefore, despite millennia of cohabitation and close interaction, the host and its native community controls and limits the assimilation of new microbes, even if closely related. Higher resolution metagenomic and microbial physiological studies, covering a larger mammalian diversity, should help understand how oral communities assemble, adapt, and interact with their hosts.IMPORTANCENumerous types of microbes colonize the mouth after birth and play important roles in maintaining oral health. When the microbiota-host homeostasis is perturbed, proliferation of some bacteria leads to diseases such as caries and periodontitis. Unlike the gut microbiome, the diversity of oral microbes across the mammalian evolutionary space is not understood. Our study compared the oral microbiomes of wild wolves, dogs, and apes (humans, chimpanzees, and bonobos), with the aim of identifying if microbes have been potentially exchanged between humans and dogs as a result of domestication and cohabitation. We found little if any evidence for such exchanges. The significance of our research is in finding that the oral microbiota and/or the host limit the acquisition of exogenous microbes, which is important in the context of natural exclusion of potential novel pathogens. We provide a framework for expanded higher-resolution studies across domestic and wild animals to understand resistance/resilience.