Genomic analyses of gray fox lineages suggest ancient divergence and secondary contact in the southern Great Plains

The gray fox (Urocyon cinereoargenteus) lineage diverged from all other extant canids at their most basal node and is restricted to the Americas. Previous mitochondrial analysis from coastal populations identified deeply divergent (up to 1 Mya) eastern and western lineages that predate most intraspecific splits in carnivores. We conducted genotyping by sequencing and mitochondrial analysis on gray foxes sampled across North America to determine geographic concordance between nuclear and mitochondrial contact zones and divergence times. We also estimated the admixture within the contact zone between eastern and western gray foxes based on nuclear DNA. Both datasets confirmed that eastern and western lineages met in the southern Great Plains (i.e. Texas and Oklahoma), where they maintained high differentiation. Admixture was generally low, with the majority of admixed individuals carrying \u3c10% ancestry from the other lineage. Divergence times confirmed a mid-Pleistocene split, similar to the mitochondrial estimates. Taken together, findings suggest gray fox lineages represent an ancient divergence event, far older than most intraspecific divergences in North American carnivores. Low admixture may reflect a relatively recent time since secondary contact (e.g. post-Pleistocene) or, alternatively, ecological or reproductive barriers between lineages. Though further research is needed to disentangle these factors, our genomic investigation suggests species-level divergence exists between eastern and western gray fox lineages

Individual Behaviors Dominate the Dynamics of an Urban Mountain Lion Population Isolated by Roads

SummaryLarge carnivores can be particularly sensitive to the effects of habitat fragmentation on genetic diversity [1, 2]. The Santa Monica Mountains (SMMs), a large natural area within Greater Los Angeles, is completely isolated by urban development and the 101 freeway to the north. Yet the SMMs support a population of mountain lions (Puma concolor), a very rare example of a large carnivore persisting within the boundaries of a megacity. GPS locations of radio-collared lions indicate that freeways are a near-absolute barrier to movement. We genotyped 42 lions using 54 microsatellite loci and found that genetic diversity in SMM lions, prior to 2009, was lower than that for any population in North America except in southern Florida, where inbreeding depression led to reproductive failure [3–5]. We document multiple instances of father-daughter inbreeding and high levels of intraspecific strife, including the unexpected behavior of a male killing two of his offspring and a mate and his son killing two of his brothers. Overall, no individuals from the SMMs have successfully dispersed. Gene flow is critical for this population, and we show that a single male immigrated in 2009, successfully mated, and substantially enhanced genetic diversity. Our results imply that individual behaviors, most likely caused by limited area and reduced opportunities to disperse, may dominate the fate of small, isolated populations of large carnivores. Consequently, comprehensive behavioral monitoring can suggest novel solutions for the persistence of small populations, such as the transfer of individuals across dispersal barriers

Extinction vortex dynamics of top predators isolated by urbanization

Extinction risk is elevated in small, isolated populations due to demographic and genetic interactions. Therefore, it is critical to model these processes realistically in population viability analyses (PVA) to inform local management and contribute to a greater understanding of mechanisms within the extinction vortex. We conducted PVA’s for two small mountain lion populations isolated by urbanization in southern California to predict population growth, extinction probability, and loss of genetic diversity with empirical data. Specifically, we (1) provide the first PVA for isolated mountain lions in the Santa Ana Mountains (SAM) that considers both demographic and genetic risk factors and (2) test the hypothesis that variation in abundance and mortality between the SAM and Santa Monica Mountains (SMM) result in differences in population growth, loss of heterozygosity, and extinction probability. Our models predicted 16–21% probability of local extinction in the SAM due purely to demographic processes over 50 yr with current low levels or no immigration. Our models also predicted that genetic diversity will further erode in the SAM such that concern regarding inbreeding depression is warranted unless gene flow is increased, and that if inbreeding depression occurs, rapid local extinction will be highly likely. Dynamics of the two populations were broadly similar, but they also exhibited differences driven by larger population size and higher mortality in the SAM. Density-independent scenarios predicted a rapidly increasing population in the SMM, whereas growth potential did not differ from a stable trend in the SAM. Demographic extinction probability and loss of heterozygosity were greater in the SMM for density-dependent scenarios without immigration. However, higher levels of immigration had stronger, positive influences on both demographic viability and retention of genetic diversity in the SMM driven by lower abundance and higher adult survival. Our results elucidate demographic and genetic threats to small populations within the extinction vortex, and how these vary relative to demographic structure. Importantly, simulating seemingly attainable increases in connectivity was sufficient to greatly reduce extinction probability. Our work highlights that conservation of large carnivores is achievable within urbanized landscapes, but requires land protection, connectivity, and strategies to promote coexistence with humans

Wild Felids as Hosts for Human Plague, Western United States

Plague seroprevalence was estimated in populations of pumas and bobcats in the western United States. High levels of exposure in plague-endemic regions indicate the need to consider the ecology and pathobiology of plague in nondomestic felid hosts to better understand the role of these species in disease persistence and transmission

Survival and competing mortality risks of mountain lions in a major metropolitan area

Understanding natural and human-caused mortality for top predators persisting in human-dominated landscapes is critical for conserving their populations. We estimated survival and cause-specific mortality rates and investigated factors influencing mortality risk of mountain lions by radio-tracking 58 individuals (33 males, 25 females) across the highly fragmented landscape in greater Los Angeles, California from 2002 to 2019. Mortality risk did not differ strongly between subadults (annual survival [ŝ]=0.68, SE=0.08) and adults (ŝ=0.81, SE=0.04). However, the different age-classes were subjected to mortality risks from different sources as subadults were more likely to be killed by conspecifics, whereas adults were more likely to die from human-caused mortality. Male subadults were frequently killed by territorial adult males in the isolated Santa Monica Mountains, mortality that may be exacerbated by substantial anthropogenic barriers to dispersal in this landscape. We also tracked kittens tagged at natal dens in the Santa Monica Mountains and estimated survival to independence to be 0.63 (SE=0.13). Higher mortality from anthropogenic causes for adults, whose survival has the greatest influence on population growth and extinction probability for mountain lions, highlights the importance of mitigation strategies to reduce human-caused mortality. Our work provides novel information about patterns of survival and mortality of mountain lions from the most urbanized landscape occupied by large carnivores in North America

Mountain lions reduce movement, increase efficiency during the Covid-19 shutdown

1. Wildlife strongly alter behaviour in response to human disturbance; however, fundamental questions remain regarding the influence of human infrastructure and activity on animal movement. The Covid-19 pandemic created a natural experiment providing an opportunity to evaluate wildlife movement during a period of greatly reduced human activity. Speculation in scientific reviews and the media suggested that wildlife might be increasing movement and colonizing urban landscapes during pandemic slowdowns. However, theory predicts that animals should move and use space as efficiently as possible, suggesting that movement might actually be reduced relative to decreased human activity. 2. We quantified space use, movement, and resource-selection of 12 GPS-collared mountain lions (eight females, four males) occupying parklands in greater Los Angeles during the Spring 2020 California stay-at-home order when human activity was far below normal. We also tested the hypothesis that reduced traffic on Los Angeles area roadways increased permeability of these barriers to animal movement. 3. Contrary to expectations that wildlife roamed more widely during pandemic shutdowns, resident mountain lions used smaller areas and moved shorter distances relative to their historical behaviour in greater Los Angeles. They also relaxed avoidance of anthropogenic landscape features such as trails and development, which likely facilitated increased travelling efficiency. However, there was no detectable change in road-crossing, despite reduced traffic volume. 4. Our results support the theoretical prediction that animals maximize movement efficiency and suggest that carnivores incur energetic costs while avoiding humans. While mountain lions may restrict movement at the landscape level relative to barriers, they appear to increase distances moved at finer scales when avoiding human activity – highlighting the scale-dependent nature of animal responses to human disturbance. 5. Avoiding humans can reduce direct mortality of large carnivores and is often suggested to be an important mechanism promoting coexistence in shared landscapes. However, energetic costs incurred by increased movement and space-use while avoiding human activity may have important consequences for population viability, predator–prey interactions, community structure, and human–wildlife conflict. Management providing sufficient wild prey and education regarding best practices for protection of domestic animals are important for conserving large carnivores in human-dominated landscapes

Extinction vortex dynamics of top predators isolated by urbanization

Extinction risk is elevated in small, isolated populations due to demographic and genetic interactions. Therefore, it is critical to model these processes realistically in population viability analyses (PVA) to inform local management and contribute to a greater understanding of mechanisms within the extinction vortex. We conducted PVA’s for two small mountain lion populations isolated by urbanization in southern California to predict population growth, extinction probability, and loss of genetic diversity with empirical data. Specifically, we (1) provide the first PVA for isolated mountain lions in the Santa Ana Mountains (SAM) that considers both demographic and genetic risk factors and (2) test the hypothesis that variation in abundance and mortality between the SAM and Santa Monica Mountains (SMM) result in differences in population growth, loss of heterozygosity, and extinction probability. Our models predicted 16–21% probability of local extinction in the SAM due purely to demographic processes over 50 yr with current low levels or no immigration. Our models also predicted that genetic diversity will further erode in the SAM such that concern regarding inbreeding depression is warranted unless gene flow is increased, and that if inbreeding depression occurs, rapid local extinction will be highly likely. Dynamics of the two populations were broadly similar, but they also exhibited differences driven by larger population size and higher mortality in the SAM. Density-independent scenarios predicted a rapidly increasing population in the SMM, whereas growth potential did not differ from a stable trend in the SAM. Demographic extinction probability and loss of heterozygosity were greater in the SMM for density-dependent scenarios without immigration. However, higher levels of immigration had stronger, positive influences on both demographic viability and retention of genetic diversity in the SMM driven by lower abundance and higher adult survival. Our results elucidate demographic and genetic threats to small populations within the extinction vortex, and how these vary relative to demographic structure. Importantly, simulating seemingly attainable increases in connectivity was sufficient to greatly reduce extinction probability. Our work highlights that conservation of large carnivores is achievable within urbanized landscapes, but requires land protection, connectivity, and strategies to promote coexistence with humans

Data from: Genome-wide expression reveals multiple systemic effects associated with detection of anticoagulant poisons in bobcats (Lynx rufus)

Anticoagulant rodenticides (ARs) are indiscriminate toxicants that threaten non-target predatory and scavenger species through secondary poisoning. Accumulating evidence suggests that AR exposure may have disruptive sublethal consequences on individuals that can affect fitness. We evaluated AR-related effects on genome wide expression patterns in a population of bobcats in southern California. We identify differential expression of genes involved in xenobiotic metabolism, endoplasmic reticulum stress response, epithelial integrity, and both adaptive and innate immune function. Further, we find that differential expression of immune related genes may be attributable to AR-related effects on leukocyte differentiation. Collectively, our results provide an unprecedented understanding of the sublethal effects of AR exposure on a wild carnivore. These findings highlight potential detrimental effects of ARs on a wide variety of species worldwide that may consume poisoned rodents and indicate the need to investigate gene expression effects of other toxicants added to natural environments by humans

Data from: Interactions between demography, genetics, and landscape connectivity increase extinction probability for a small population of large carnivores in a major metropolitan area

The extinction vortex is a theoretical model describing the process by which extinction risk is elevated in small, isolated populations owing to interactions between environmental, demographic, and genetic factors. However, empirical demonstrations of these interactions have been elusive. We modelled the dynamics of a small mountain lion population isolated by anthropogenic barriers in greater Los Angeles, California, to evaluate the influence of demographic, genetic, and landscape factors on extinction probability. The population exhibited strong survival and reproduction, and the model predicted stable median population growth and a 15% probability of extinction over 50 years in the absence of inbreeding depression. However, our model also predicted the population will lose 40–57% of its heterozygosity in 50 years. When we reduced demographic parameters proportional to reductions documented in another wild population of mountain lions that experienced inbreeding depression, extinction probability rose to 99.7%. Simulating greater landscape connectivity by increasing immigration to greater than or equal to one migrant per generation appears sufficient to largely maintain genetic diversity and reduce extinction probability. We provide empirical support for the central tenet of the extinction vortex as interactions between genetics and demography greatly increased extinction probability relative to the risk from demographic and environmental stochasticity alone. Our modelling approach realistically integrates demographic and genetic data to provide a comprehensive assessment of factors threatening small populations

Data from: Urbanization and anticoagulant poisons promote immune dysfunction in bobcats

Understanding how human activities influence immune response to environmental stressors can support biodiversity conservation across increasingly urbanizing landscapes. We studied a bobcat (Lynx rufus) population in urban southern California that experienced a rapid population decline from 2002–2005 due to notoedric mange. Because anticoagulant rodenticide (AR) exposure was an underlying complication in mange deaths, we aimed to understand sublethal contributions of urbanization and ARs on 65 biochemical markers of immune and organ function. Variance in immunological variables was primarily associated with AR exposure and secondarily with urbanization. Use of urban habitat and AR exposure has pervasive, complex and predictable effects on biochemical markers of immune and organ function in free-ranging bobcats that include impacts on neutrophil, lymphocyte and cytokine populations, total bilirubin and phosphorus. We find evidence of both inflammatory response and immune suppression associated with urban land use and rat poison exposure that could influence susceptibility to opportunistic infections. Consequently, AR exposure may influence mortality and has population-level effects, as previous work in the focal population has revealed substantial mortality caused by mange infection. The secondary effects of anticoagulant exposure may be a worldwide, largely unrecognized problem affecting a variety of vertebrate species in human-dominated environments