Captive Breeding Protocols and Their Impact on Genetic Diversity in White-footed Mice (Peromyscus leucopus): Implications for Threatened and Endangered Species

Captive breeding protocols used in zoos often are aimed at increasing population sizes and retaining genetic diversity of endangered species. However, captive breeding causes genetic adaptation to captivity that can lead to an overall decrease in genetic diversity and reduce chances of a successful reintroduction to the wild. In this study, we assess how 3 different breeding protocols—random mating, preferential breeding of individuals with the lowest mean kinship scores, and selection for docility—affect the variability of mitochondrial DNA in white-footed mice (Peromyscus leucopus). We used mice that were captured from the wild but were mated for up to 20 generations using one of the aforementioned breeding protocols. Using animals from generations 0, 6, and 19, as well as the wild source population, we sequenced the mitochondrial D-loop in 2 replicate populations representing each of the 3 breeding protocols. Initial sequences indicate there is genetic variation at this mitochondrial locus, and further sequencing will allow us to quantify the genetic diversity maintained under each breeding protocol. These results will increase our understanding of the decline in genetic diversity due to adaptation to captivity. Thus, our results will have direct relevance for the maintenance and growth of zoo populations of critically endangered species

Segregating the effects of seed traits and common ancestry of hardwood trees on eastern gray squirrel foraging decisions

The evolution of specific seed traits in scatter-hoarded tree species often has been attributed to granivore foraging behavior. However, the degree to which foraging investments and seed traits correlate with phylogenetic relationships among trees remains unexplored. We presented seeds of 23 different hardwood tree species (families Betulaceae, Fagaceae, Juglandaceae) to eastern gray squirrels (Sciurus carolinensis), and measured the time and distance travelled by squirrels that consumed or cached each seed. We estimated 11 physical and chemical seed traits for each species, and the phylogenetic relationships between the 23 hardwood trees. Variance partitioning revealed that considerable variation in foraging investment was attributable to seed traits alone (27-73%), and combined effects of seed traits and phylogeny of hardwood trees (5-55%). A phylogenetic PCA (pPCA) on seed traits and tree phylogeny resulted in 2 global axes of traits that were phylogenetically autocorrelated at the family and genus level and a third local axis in which traits were not phylogenetically autocorrelated. Collectively, these axes explained 30-76% of the variation in squirrel foraging investments. The first global pPCA axis, which produced large scores for seed species with thin shells, low lipid and high carbohydrate content, was negatively related to time to consume and cache seeds and travel distance to cache. The second global pPCA axis, which produced large scores for seeds with high protein, low tannin and low dormancy levels, was an important predictor of consumption time only. The local pPCA axis primarily reflected kernel mass. Although it explained only 12% of the variation in trait space and was not autocorrelated among phylogenetic clades, the local axis was related to all four squirrel foraging investments. Squirrel foraging behaviors are influenced by a combination of phylogenetically conserved and more evolutionarily labile seed traits that is consistent with a weak or more diffuse coevolutionary relationship between rodents and hardwood trees rather than a direct coevolutionary relationship. © 2015 Sundaram et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

Incipient resistance to an effective pesticide results from genetic adaptation and the canalization of gene expression

The resistance of pest species to chemical controls has vast ecological, economic, and societal costs. In most cases, resistance is only detected after spreading throughout an entire population. Detecting resistance in its incipient stages, by comparison, provides time to implement preventative strategies. Incipient resistance can be detected by coupling standard toxicology assays with large-scale gene expression experiments. We apply this approach to a system where an invasive parasite, sea lamprey (Petromyzon marinus), has been treated with the highly effective pesticide 3-trifluoromethyl-4-nitrophenol (TFM) for 60 years. Toxicological experiments revealed that lamprey from treated populations did not have higher survival to TFM exposure than lamprey from untreated populations, demonstrating that full-fledged resistance has not yet evolved. In contrast, we find hundreds of genes differentially expressed in response to TFM in the population with the longest history of exposure, many of which relate to TFM's primary mode of action, the uncoupling of oxidative phosphorylation, and subsequent depletion of ATP. Three genes critical to oxidative phosphorylation, ATP5PB, PLCB1, and NDUFA9, were nearly fixed for alternative alleles in comparisons of SNPs between treated and untreated populations (FST > 5 SD from the mean). ATP5PB encodes subunit b of ATP synthase and an additional subunit, ATP5F1B, was canalized for high expression in treated populations, but remained plastic in response to TFM treatment in individuals from the untreated population. These combined genomic and transcriptomic results demonstrate that an adaptive, genetic response to TFM is likely driving incipient resistance in a damaging pest species

2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education.

Guidelines for use of wild mammal species in research are updated from Sikes et al. (2011). These guidelines cover current professional techniques and regulations involving the use of mammals in research and teaching; they also incorporate new resources, procedural summaries, and reporting requirements. Included are details on capturing, marking, housing, and humanely killing wild mammals. It is recommended that Institutional Animal Care and Use Committees (IACUCs), regulatory agencies, and investigators use these guidelines as a resource for protocols involving wild mammals, whether studied in the field or in captivity. These guidelines were prepared and approved by the American Society of Mammalogists (ASM), in consultation with professional veterinarians experienced in wildlife research and IACUCs, whose collective expertise provides a broad and comprehensive understanding of the biology of nondomesticated mammals. The current version of these guidelines and any subsequent modifications are available online on the Animal Care and Use Committee page of the ASM website (http://mammalogy.org/uploads/committee_files/CurrentGuidelines.pdf). Additional resources pertaining to the use of wild animals in research are available at: http://www.mammalsociety.org/committees/animal-care-and-use#tab3. Resumen—Los lineamientos para el uso de especies de mamíferos de vida silvestre en la investigación con base en Sikes et al. (2011) se actualizaron. Dichos lineamientos cubren técnicas y regulaciones rofesionales actuales que involucran el uso de mamíferos en la investigación y enseñanza; también incorporan recursos nuevos, resúmenes de procedimientos y requisitos para reportes. Se incluyen detalles acerca de captura, marcaje, manutención en cautiverio y eutanasia de mamíferos de vida silvestre. Se recomienda que los comités institucionales de uso y cuidado animal (cifras en inglés: IACUCs), las agencias reguladoras y los investigadores se adhieran a dichos lineamientos como fuente base de protocolos que involucren mamíferos de vida silvestre, ya sea investigaciones de campo o en cautiverio. Dichos lineamientos fueron preparados y aprobados por la ASM, en consulta con profesionales veterinarios experimentados en investigaciones de vida silvestre y IACUCS, de quienes cuya experiencia colectiva provee un entendimiento amplio y exhaustivo de la biología de mamíferos no-domesticados. La presente version de los lineamientos y modificaciones posteriores están disponibles en línea en la página web de la ASM, bajo Cuidado Animal y Comité de Uso: http://mammalogy.org/uploads/committee_files/CurrentGuidelines.pdf). Recursos adicionales relacionados con el uso de animales de vida silvestre para la investigación se encuentran disponibles en (http://www.mammalsociety.org/committees/animal-care-and-use#tab3)

Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis.

Multiple sclerosis is a common disease of the central nervous system in which the interplay between inflammatory and neurodegenerative processes typically results in intermittent neurological disturbance followed by progressive accumulation of disability. Epidemiological studies have shown that genetic factors are primarily responsible for the substantially increased frequency of the disease seen in the relatives of affected individuals, and systematic attempts to identify linkage in multiplex families have confirmed that variation within the major histocompatibility complex (MHC) exerts the greatest individual effect on risk. Modestly powered genome-wide association studies (GWAS) have enabled more than 20 additional risk loci to be identified and have shown that multiple variants exerting modest individual effects have a key role in disease susceptibility. Most of the genetic architecture underlying susceptibility to the disease remains to be defined and is anticipated to require the analysis of sample sizes that are beyond the numbers currently available to individual research groups. In a collaborative GWAS involving 9,772 cases of European descent collected by 23 research groups working in 15 different countries, we have replicated almost all of the previously suggested associations and identified at least a further 29 novel susceptibility loci. Within the MHC we have refined the identity of the HLA-DRB1 risk alleles and confirmed that variation in the HLA-A gene underlies the independent protective effect attributable to the class I region. Immunologically relevant genes are significantly overrepresented among those mapping close to the identified loci and particularly implicate T-helper-cell differentiation in the pathogenesis of multiple sclerosis

Genetic diversity in animal populations: Patterns, processes, and applications to conservation

Using a combination of genetic and genomic tools, I have investigated how species traits influence patterns of genetic diversity (GD), the genetic and genomic impacts of captive breeding, and the methods required for genetic sampling via environmental samples. In chapter two, I found that migratory vertebrates harbor less contemporary GD compared to non-migratory species and compare these trends between Classes and amongst dominant biomes in which the species reside. I found that the effect of migratory behavior on genetic diversity varies between vertebrate classes as does the biome in which the species occurs. In my third chapter, I use the same taxa delineations to investigate the relationship between conservation status and genetic diversity. I found that GD was typically smaller in threatened species relative to species of lesser conservation concern; I also propose a new method for identifying species of concern based on reduced GD. In chapters four and five, I compare the change in GD that occurs when populations are bred in captivity using multiple breeding protocols. Using microsatellites, mtDNA sequences, SNPs, and pedigrees, I identified the protocol that resulted in the slowest loss of GD due to reduced inbreeding and selection. However, I found that the effects of drift were not sufficiently mitigated in any captive population. Finally in chapter six, I review the published eDNA literature and determine the experimental factors that contribute to detection of target species. From these patterns, I suggest a method based on site-occupancy models for estimating required sampling effort

Data from: Captive ancestry upwardly biases estimates of relative reproductive success

Supplementation programs, which release captive-born individuals into the wild, are commonly used to demographically bolster declining populations. In order to evaluate the effectiveness of these programs, the reproductive success of captive-born individuals released into the wild is often compared to the reproductive success of wild-born individuals in the recipient population (relative reproductive success, RRS). However, if there are heritable reductions in fitness associated with captive breeding, gene flow from captive-born individuals into the wild population can reduce the fitness of the wild population. Here, we show that when captive ancestry in the wild population reduces mean population fitness, estimates of RRS are upwardly biased, meaning that the relative fitness of captive-born individuals is over-estimated. Furthermore, the magnitude of this bias increases with the length of time that a supplementation program has been releasing captive-born individuals. This phenomenon has long-term conservation impacts since management decisions regarding the design of a supplementation program and the number of individuals to release can be based, at least in part, on RRS estimates. Therefore, we urge caution in the interpretation of relative fitness measures when the captive ancestry of the wild population cannot be precisely measured

Comparison of Minimally Invasive Monitoring Methods and Live Trapping in Mammals

The conservation and management of wildlife requires the accurate assessment of wildlife population sizes. However, there is a lack of synthesis of research that compares methods used to estimate population size in the wild. Using a meta-analysis approach, we compared the number of detected individuals in a study made using live trapping and less invasive approaches, such as camera trapping and genetic identification. We scanned 668 papers related to these methods and identified data for 44 populations (all focused on mammals) wherein at least two methods (live trapping, camera trapping, genetic identification) were used. We used these data to quantify the difference in number of individuals detected using trapping and less invasive methods using a regression and used the residuals from each regression to evaluate potential drivers of these trends. We found that both trapping and less invasive methods (camera traps and genetic analyses) produced similar estimates overall, but less invasive methods tended to detect more individuals compared to trapping efforts (mean = 3.17 more individuals). We also found that the method by which camera data are analyzed can significantly alter estimates of population size, such that the inclusion of spatial information was related to larger population size estimates. Finally, we compared counts of individuals made using camera traps and genetic data and found that estimates were similar but that genetic approaches identified more individuals on average (mean = 9.07 individuals). Overall, our data suggest that all of the methods used in the studies we reviewed detected similar numbers of individuals. As live trapping can be more costly than less invasive methods and can pose more risk to animal well-fare, we suggest minimally invasive methods are preferable for population monitoring when less-invasive methods can be deployed efficiently

simulations

Code, inputfiles, and output files from simulation of mean kinship, random mating, and selecting for docility in captive populations. Code (simulations.R) was written for R, and has a number of package dependencies listed at the top. Also required to run the code are the input cdv files: Weanded.csv lists number of individuals weaned in each population, founders.csv contains microsatellite genotypes for the populations founders, and mtDNA.csv contains the dloop haplotypes for each founder. Docility.txt, MeanKinship.txt, MKplus.txt, and RandomMating.txt are all output files from running the simulation code

Decline of heterozygosity in a large but isolated population: a 45-year examination of moose genetic diversity on Isle Royale

Wildlife conservation and management approaches typically focus on demographic measurements to assess population viability over both short and long periods. However, genetic diversity is an important predictor of long term population vitality. We investigated the pattern of change in genetic diversity in a large and likely isolated moose (Alces alces) population on Isle Royale (Lake Superior) from 1960–2005. We characterized samples, partitioned into five different 5-year periods, using nine microsatellite loci and a portion of the mtDNA control region. We also simulated the moose population to generate a theoretical backdrop of genetic diversity change. In the empirical data, we found that the number of alleles was consistently low and that observed heterozygosity notably declined from 1960 to 2005 (p = 0.08, R2 = 0.70). Furthermore, inbreeding coefficients approximately doubled from 0.08 in 1960–65 to 0.16 in 2000–05. Finally, we found that the empirical rate of observed heterozygosity decline was faster than the rate of observed heterozygosity loss in our simulations. Combined, these data suggest that genetic drift and inbreeding occurred in the Isle Royale moose populations over the study period, leading to significant losses in heterozygosity. Although inbreeding can be mitigated by migration, we found no evidence to support the occurrence of recent migrants into the population using analysis of our mtDNA haplotypes nor microsatellite data. Therefore, the Isle Royale moose population illustrates that even large populations are subjected to inbreeding in the absence of migration