Holly B. Ernest

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.

Multi-level, multi-scale resource selection functions and resistance surfaces for conservation planning: Pumas as a case study

The importance of examining multiple hierarchical levels when modeling resource use for wildlife has been acknowledged for decades. Multi-level resource selection functions have recently been promoted as a method to synthesize resource use across nested organizational levels into a single predictive surface. Analyzing multiple scales of selection within each hierarchical level further strengthens multi-level resource selection functions. We extend this multi-level, multi-scale framework to modeling resistance for wildlife by combining multi-scale resistance surfaces from two data types, genetic and movement. Resistance estimation has typically been conducted with one of these data types, or compared between the two. However, we contend it is not an either/or issue and that resistance may be better-modeled using a combination of resistance surfaces that represent processes at different hierarchical levels. Resistance surfaces estimated from genetic data characterize temporally broad-scale dispersal and successful breeding over generations, whereas resistance surfaces estimated from movement data represent fine-scale travel and contextualized movement decisions. We used telemetry and genetic data from a long-term study on pumas (Puma concolor) in a highly developed landscape in southern California to develop a multi-level, multi-scale resource selection function and a multi-level, multi-scale resistance surface. We used these multi-level, multi-scale surfaces to identify resource use patches and resistant kernel corridors. Across levels, we found puma avoided urban, agricultural areas, and roads and preferred riparian areas and more rugged terrain. For other landscape features, selection differed among levels, as did the scales of selection for each feature. With these results, we developed a conservation plan for one of the most isolated puma populations in the U.S. Our approach captured a wide spectrum of ecological relationships for a population, resulted in effective conservation planning, and can be readily applied to other wildlife species.

Genetic sequence data reveals widespread sharing of Leucocytozoon lineages in corvids

Leucocytozoon, a widespread hemosporidian blood parasite that infects a broad group of avian families, has been studied in corvids (family: Corvidae) for over a century. Current taxonomic classification indicates that Leucocytozoon sakharoffi infects crows and related Corvus spp., while Leucocytozoon berestneffi infects magpies (Pica spp.) and blue jays (Cyanocitta sp.). This intrafamily host specificity was based on the experimental transmissibility of the parasites, as well as slight differences in their morphology and life cycle development. Genetic sequence data from Leucocytozoon spp. infecting corvids is scarce, and until the present study, sequence data has not been analyzed to confirm the current taxonomic distinctions. Here, we predict the phylogenetic relationships of Leucocytozoon cytochrome b lineages recovered from infected American Crows (Corvus brachyrhynchos), yellow-billed magpies (Pica nuttalli), and Steller’s jays (Cyanocitta stelleri) to explore the host specificity pattern of L. sakharoffi and L. berestneffi. Phylogenetic reconstruction revealed a single large clade containing nearly every lineage recovered from the three host species, while showing no evidence of the expected distinction between L. sakharoffi and L. berestneffi. In addition, five of the detected lineages were recovered from both crows and magpies. This absence of the previously described host specificity in corvid Leucocytozoon spp. suggests that L. sakharoffi and L. berestneffi be reexamined from a taxonomic perspective.

A single migrant enhances the genetic diversity of an inbred puma population

Migration is essential for maintaining genetic diversity among populations, and pumas (Puma concolor) provide an excellent model for studying the genetic impacts of migrants on populations isolated by increasing human development. In densely populated southern California, USA, puma populations on the east and west side of interstate highway 15 (I-15) have become fragmented into a small inbred population on the west side (Santa Ana Mountains) and a relatively larger, more diverse population on the east side (Eastern Peninsular Range). From 146 sampled pumas, genetic analyses indicate seven pumas crossed I-15 over the last 15 years, including four males from west to east, and three males from east to west. However, only a single migrant (named M86) was detected to have produced offspring and contribute to gene flow across the I-15 barrier. Prior to the M86 migration, the Santa Ana population exhibited inbreeding and had significantly lower genetic diversity than the Eastern Peninsular Range population. After M86 emigrated, he sired 11 offspring with Santa Ana females, decreasing inbreeding measures and raising heterozygosity to levels similar to pumas in the Eastern Peninsular Range. The emigration of M86 also introduced new alleles into the Santa Ana population, although allelic richness still remained significantly lower than the Eastern Peninsular population. Our results clearly show the benefit of a single migrant to the genetics of a small, isolated population. However, ongoing development and habitat loss on both sides of I-15 will increasingly strengthen the barrier to successful migration. Further monitoring, and potential human intervention, including minimizing development effects on connectivity, adding or improving freeway crossing structures, or animal translocation, may be needed to ensure adequate gene flow and long-term persistence of the Santa Ana puma population.

Sea Otter Conservation Genetics

Conservation genetics is the science focused on the understanding of hereditary processes and mitigating factors that endanger populations at risk of extinction. It is an interdisciplinary specialty in which geneticists explore genetic variation, with the goal of enabling resource managers to better conserve biodiversity. Sea otters offer a unique case for the study and application of conservation genetics because of their documented history of population reduction and recovery from the fur trade of the eighteenth and nineteenth centuries. Population genetic studies using microsatellites and mitochondrial (mt) DNA have found low genetic diversity within modern sea otters compared to those sampled during the fur trade. Many sea otter populations remain fragmented and isolated today, more than 100 years after the fur trade ended, although they maintain historical genetic structuring based on analysis of both pre- and post-fur trade populations. Translocations to augment recovery in areas where sea otters remained absent have resulted in recovery of some of the lost genetic diversity. In addition to studies of genetic diversity, genetic methods such as allozymes, mtDNA restriction fragment-length polymorphism (RFLP) analysis, microsatellites, and direct sequencing have been used to determine genetically distinct populations and stocks to inform management decisions. Newer research on adaptive genetics has investigated portions of the genome responsible for individual and population health, such as the major histocompatibility complex (MHC) and gene expression, reporting varying levels of diversity and expression. Here we review the methods and results of past genetic studies, explore future directions for sea otter conservation genetics, and discuss the implications of genetic research for the long-term conservation of sea otter populations.

Leukocyte Reference Intervals for Free-Ranging Hummingbirds in Northern California, USA

Abstract:  Hummingbirds are specialized nectarivores and important ecological pollinators that are the focus of conservation efforts as well as scientific investigations of metabolism and flight dynamics. Despite their importance, basic information is lacking about hummingbird blood cells. We aimed to establish reference intervals for total and differential leukocyte counts from healthy free-ranging hummingbirds in northern California. Hummingbirds were captured in four counties in spring and summer of 2012. A drop of blood was used to prepare smears for total white blood cell estimate and 200-cell differential leukocyte counts. Reference Value Advisor was used for descriptive statistics and calculation of reference intervals. Blood smears from 42 Annas Hummingbirds (Calypte anna) and 33 Black-chinned Hummingbirds (Archilochus alexandri) were included. The only significant differences in leukocyte counts were due to age, and juvenile hummingbirds had significantly higher lymphocyte counts than adult hummingbirds (P<0.0001). These reference intervals provide robust baseline data to evaluate health status and disease in free-ranging hummingbirds.

Pathogens in space: Advancing understanding of pathogen dynamics and disease ecology through landscape genetics

Landscape genetics has provided many insights into how heterogeneous landscape features drive processes influencing spatial genetic variation in free‐living organisms. This rapidly developing field has focused heavily on vertebrates, and expansion of this scope to the study of infectious diseases holds great potential for landscape geneticists and disease ecologists alike. The potential application of landscape genetics to infectious agents has garnered attention at formative stages in the development of landscape genetics, but systematic examination is lacking. We comprehensively review how landscape genetics is being used to better understand pathogen dynamics. We characterize the field and evaluate the types of questions addressed, approaches used and systems studied. We also review the now established landscape genetic methods and their realized and potential applications to disease ecology. Lastly, we identify emerging frontiers in the landscape genetic study of infectious agents, including recent phylogeographic approaches and frameworks for studying complex multihost and host‐vector systems. Our review emphasizes the expanding utility of landscape genetic methods available for elucidating key pathogen dynamics (particularly transmission and spread) and also how landscape genetic studies of pathogens can provide insight into host population dynamics. Through this review, we convey how increasing awareness of the complementarity of landscape genetics and disease ecology among practitioners of each field promises to drive important cross‐disciplinary advances.

Founder events, isolation, and inbreeding: Intercontinental genetic structure of the domestic ferret

Domestication and breeding for human‐desired morphological traits can reduce population genetic diversity via founder events and artificial selection, resulting in inbreeding depression and genetic disorders. The ferret (Mustela putorius furo) was domesticated from European polecats (M. putorius), transported to multiple continents, and has been artificially selected for several traits. The ferret is now a common pet, a laboratory model organism, and feral ferrets can impact native biodiversity. We hypothesized global ferret trade resulted in distinct international genetic clusters and that ferrets transported to other continents would have lower genetic diversity than ferrets from Europe because of extreme founder events and no hybridization with wild polecats or genetically diverse ferrets. To assess these hypotheses, we genotyped 765 ferrets at 31 microsatellites from 11 countries among the continents of North America, Europe, and Australia and estimated population structure and genetic diversity. Fifteen M. putorius were genotyped for comparison. Our study indicated ferrets exhibit geographically distinct clusters and highlights the low genetic variation in certain countries. Australian and North American clusters have the lowest genetic diversities and highest inbreeding metrics whereas the United Kingdom (UK) cluster exhibited intermediate genetic diversity. Non‐UK European ferrets had high genetic diversity, possibly a result of introgression with wild polecats. Notably, Hungarian ferrets had the highest genetic diversity and Hungary is the only country sampled with two wild polecat species. Our research has broad social, economic, and biomedical importance. Ferret owners and veterinarians should be made aware of potential inbreeding depression. Breeders in North America and Australia would benefit by incorporating genetically diverse ferrets from mainland Europe. Laboratories using ferrets as biomedical organisms should consider diversifying their genetic stock and incorporating genetic information into bioassays. These results also have forensic applications for conserving the genetics of wild polecat species and for identifying and managing sources of feral ferrets causing ecosystem damage.

Measures of effective population size in sea otters reveal special considerations for wide-ranging species

Conservation genetic techniques and considerations of the evolutionary potential of a species are increasingly being applied to species conservation. For example, effective population size (Ne) estimates are useful for determining the conservation status of species, yet accurate estimates of current Ne remain difficult to obtain. The effective population size can contribute to setting federal delisting criteria, as was done for the southern sea otter (Enhydra lutris nereis). After being hunted to near extinction during the North Pacific fur trade, the southern sea otter has recovered over part of its former range, but remains at relatively low numbers, making it desirable to obtain accurate and consistent estimates of Ne. Although theoretical papers have compared the validity of several methods, comparisons of estimators using empirical data in applied conservation settings are limited. We combined thirteen years of demographic and genetic data from 1,006 sea otters to assess multiple Ne estimators, as well as temporal trends in genetic diversity and population genetic structure. Genetic diversity was low and did not increase over time. There was no evidence for distinct genetic units, but some evidence for genetic isolation by distance. In particular, estimates of Ne based on demographic data were much larger than genetic estimates when computed for the entire range of the population, but were similar at smaller spatial scales. The discrepancy between estimates at large spatial scales could be driven by cryptic population structure and/or individual differences in reproductive success. We recommend the development of new delisting criteria for the southern sea otter. We advise the use of multiple estimates of Ne for other wide‐ranging species, species with overlapping generations, or with sex‐biased dispersal, as well as the development of improved metrics of genetic assessments of populations.

Mitogenomes and relatedness do not predict frequency of tool-use by sea otters

Many ecological aspects of tool-use in sea otters are similar to those in Indo-Pacific bottlenose dolphins. Within an area, most tool-using dolphins share a single mitochondrial haplotype and are more related to each other than to the population as a whole. We asked whether sea otters in California showed similar genetic patterns by sequencing mitogenomes of 43 otters and genotyping 154 otters at 38 microsatellite loci. There were six variable sites in the mitogenome that yielded three haplotypes, one found in only a single individual. The other two haplotypes contained similar percentages (33 and 36%) of frequent tool-users and a variety of diet types. Microsatellite analyses showed that snail specialists, the diet specialist group that most frequently used tools, were no more related to each other than to the population as a whole. The lack of genetic association among tool-using sea otters compared with dolphins may result from the length of time each species has been using tools. Tool-use in dolphins appears to be a relatively recent innovation (less than 200 years) but sea otters have probably been using tools for many thousands or even millions of years.