• A comparison of strategies for selecting breeding pairs to maximize genetic diversity retention in managed populations

      Ivy, Jamie A.; Lacy, Robert C. (2012)
      Captive breeding programs aim to maintain populations that are demographically self-sustaining and genetically healthy. It has been well documented that the best way for managed breeding programs to retain gene diversity (GD) and limit inbreeding is to select breeding pairs that minimize a population's average kinship....
    • A high density snp array for the domestic horse and extant Perissodactyla: Utility for association mapping, genetic diversity, and phylogeny studies

      McCue, Molly E.; Bannasch, Danika L.; Petersen, Jessica L.; Gurr, Jessica; Bailey, Ernie; Binns, Matthew M.; Distl, Ottmar; Guérin, Gérard; Hasegawa, Telhisa; Hill, Emmeline W.; et al. (2012)
      An equine SNP genotyping array was developed and evaluated on a panel of samples representing 14 domestic horse breeds and 18 evolutionarily related species. More than 54,000 polymorphic SNPs provided an average inter-SNP spacing of ?43 kb. The mean minor allele frequency across domestic horse breeds was 0.23, and the number of polymorphic SNPs within breeds ranged from 43,287 to 52,085. Genome-wide linkage disequilibrium (LD) in most breeds declined rapidly over the first 50–100 kb and reached background levels within 1–2 Mb. The extent of LD and the level of inbreeding were highest in the Thoroughbred and lowest in the Mongolian and Quarter Horse. Multidimensional scaling (MDS) analyses demonstrated the tight grouping of individuals within most breeds, close proximity of related breeds, and less tight grouping in admixed breeds. The close relationship between the Przewalski's Horse and the domestic horse was demonstrated by pair-wise genetic distance and MDS. Genotyping of other Perissodactyla (zebras, asses, tapirs, and rhinoceros) was variably successful, with call rates and the number of polymorphic loci varying across taxa. Parsimony analysis placed the modern horse as sister taxa to Equus przewalski. The utility of the SNP array in genome-wide association was confirmed by mapping the known recessive chestnut coat color locus (MC1R) and defining a conserved haplotype of -750 kb across all breeds. These results demonstrate the high quality of this SNP genotyping resource, its usefulness in diverse genome analyses of the horse, and potential use in related species.
    • An optimal and near-optimal strategy to selecting individuals for transfer in captive breeding programs

      Allen, S.D.; Fathi, Y.; Gross, K.; Mace, Michael E.; (2010)
      As species extinction rates continue to rise, zoos have adopted a more active role in the conservation of endangered species. A central concern is to preserve genetic diversity of zoological populations....
    • Applying SNP-derived molecular coancestry estimates to captive breeding programs

      Ivy, Jamie A.; Putnam, Andrea S.; Navarro, Asako Y.; Gurr, Jessica; Ryder, Oliver A. (2016)
      ...Although pedigree-based breeding strategies are quite effective at retaining long-term genetic variation, management of zoo-based breeding programs continues to be hampered when pedigrees are poorly known. The objective of this study was to evaluate 2 options for generating single nucleotide polymorphism (SNP) data to resolve unknown relationships within captive breeding programs...
    • Conservation genomics of threatened animal species

      Steiner, Cynthia C.; Putnam, Andrea S.; Hoeck, Paquita E. A.; Ryder, Oliver A. (2013)
      The genomics era has opened up exciting possibilities in the field of conservation biology by enabling genomic analyses of threatened species that previously were limited to model organisms. Next-generation sequencing (NGS) and the collection of genome-wide data allow for more robust studies of the demographic history of populations and adaptive variation associated with fitness and local adaptation.…
    • Deciphering genetic mate choice: Not so simple in group-housed conservation breeding programs

      Farquharson, Katherine A.; Hogg, Carolyn J.; Belov, Katherine; Grueber, Catherine E. (2020)
      Incorporating mate choice into conservation breeding programs can improve reproduction and the retention of natural behaviors. However, different types of genetic-based mate choice can have varied consequences for genetic diversity management. As a result, it is important to examine mechanisms of mate choice in captivity to assess its costs and benefits. Most research in this area has focused on experimental pairing trials; however, this resource-intensive approach is not always feasible in captive settings and can interfere with other management constraints. We used generalized linear mixed models and permutation approaches to investigate overall breeding success in group-housed Tasmanian devils at three nonmutually exclusive mate choice hypotheses: (a) advantage of heterozygous individuals, (b) advantage of dissimilar mates, and (c) optimum genetic distance, using both 1,948 genome-wide SNPs and 12 MHC-linked microsatellites. The managed devil insurance population is the largest such breeding program in Australia and is known to have high variance in reproductive success. We found that nongenetic factors such as age were the best predictors of breeding success in a competitive breeding scenario, with younger females and older males being more successful. We found no evidence of mate choice under the hypotheses tested. Mate choice varies among species and across environments, so we advocate for more studies in realistic captive management contexts as experimental or wild studies may not apply. Conservation managers must weigh up the need to wait for adequate sample sizes to detect mate choice with the risk that genetic changes may occur during this time in captivity. Our study shows that examining and integrating mate choice into the captive management of species housed in realistic, semi-natural group-based contexts may be more difficult than previously considered.
    • Demographic, environmental and genetic determinants of mating success in captive koalas (Phascolarctos cinereus)

      Abts, Kendra C.; Ivy, Jamie A.; DeWoody, J. Andrew (2018)
      Many factors have been shown to affect mating behavior. For instance, genes of the major histocompatibility complex (MHC) are known to influence mate choice in a wide variety of vertebrate species....
    • Development of a SNP-based assay for measuring genetic diversity in the Tasmanian devil insurance population

      Wright, Belinda; Morris, Katrina; Grueber, Catherine E.; Willet, Cali E.; Gooley, Rebecca; Hogg, Carolyn J.; O’Meally, Denis; Hamede, Rodrigo; Jones, Menna; Wade, Claire; et al. (2015)
      The Tasmanian devil (Sarcophilus harrisii) has undergone a recent, drastic population decline due to the highly contagious devil facial tumor disease. The tumor is one of only two naturally occurring transmissible cancers and is almost inevitably fatal. In 2006 a disease-free insurance population was established to ensure that the Tasmanian devil is protected from extinction. The insurance program is dependent upon preserving as much wild genetic diversity as possible to maximize the success of subsequent reintroductions to the wild. Accurate genotypic data is vital to the success of the program to ensure that loss of genetic diversity does not occur in captivity. Until recently, microsatellite markers have been used to study devil population genetics, however as genetic diversity is low in the devil and potentially decreasing in the captive population, a more sensitive genotyping assay is required.
    • Evaluating the performance of captive breeding techniques for conservation hatcheries: A case study of the delta smelt captive breeding program

      Fisch, Kathleen M.; Ivy, Jamie A.; Burton, Ronald S.; May, Bernie (2013)
      The delta smelt, an endangered fish species endemic to the San Francisco Bay-Delta, California, United States, was recently brought into captivity for species preservation. This study retrospectively evaluates the implementation of a genetic management plan for the captive delta smelt population....
    • Fitness costs associated with ancestry to isolated populations of an endangered species

      Wilder, Aryn P.; Navarro, Asako Y.; King, Shauna N. D.; Miller, William B.; Thomas, Steven M.; Steiner, Cynthia C.; Ryder, Oliver A.; Shier, Debra M. (2020)
      ... The endangered Pacific pocket mouse (Perognathus longimembris pacificus) persists in three isolated populations in southern California. Mitochondrial and microsatellite data indicated that effective population sizes were extremely small (Ne< 50), and continued declines prompted a conservation breeding program founded by individuals from each population....
    • Genetic guidelines for maintaining a conservation collection

      Maschinski, Joyce; Havens, Kayri; Font, Jeremie; Kramer, Andrea; Vitt, Pati; Neale, Jennifer Ramp; Guerrant Jr., Edward O.; Edwards, Christine; Steele, Stephanie; Maschinski, Joyce; et al. (Center for Plant ConservationEscondido, California, 2019)
      Give your reintroduced population a good chance for survival by starting with adequate numbers of plants or seeds at the beginning. Determine the source of the plants or seeds. Determine whether the source should consist of seeds or plants from a single population or from mixed populations.
    • Genetic tools: maintaining genetic diversity in the Tasmanian devil metapopulation

      Grueber, Catherine E.; McLennan, Elspeth A.; Hogg, Carolyn J.; Fox, Samantha; Pemberton, David; Belov, Katherine (CSIROClayton South, Australia, 2019)
    • Inbreeding and selection shape genomic diversity in captive populations: Implications for the conservation of endangered species

      Willoughby, Janna R.; Ivy, Jamie A.; Lacy, Robert C.; Doyle, Jacqueline M.; DeWoody, J. Andrew (2017)
      Captive breeding programs are often initiated to prevent species extinction until reintroduction into the wild can occur. However, the evolution of captive populations via inbreeding, drift, and selection can impair fitness, compromising reintroduction programs. To better understand the evolutionary response of species bred in captivity, we used nearly 5500 single nucleotide polymorphisms (SNPs) in populations of white-footed mice (Peromyscus leucopus) to measure the impact of breeding regimes on genomic diversity. We bred mice in captivity for 20 generations using two replicates of three protocols: random mating (RAN), selection for docile behaviors (DOC), and minimizing mean kinship (MK). The MK protocol most effectively retained genomic diversity and reduced the effects of selection. Additionally, genomic diversity was significantly related to fitness, as assessed with pedigrees and SNPs supported with genomic sequence data. Because captive-born individuals are often less fit in wild settings compared to wild-born individuals, captive-estimated fitness correlations likely underestimate the effects in wild populations. Therefore, minimizing inbreeding and selection in captive populations is critical to increasing the probability of releasing fit individuals into the wild.
    • Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix

      Springer, Mark S.; Meredith, Robert W.; Gatesy, John; Emerling, Christopher A.; Park, Jong; Rabosky, Daniel L.; Stadler, Tanja; Steiner, Cynthia C.; Ryder, Oliver A.; Janečka, Jan E.; et al. (2012)
      Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living Primates last shared a common ancestor 71–63 Ma, and that divergences within both Strepsirrhini and Haplorhini are entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a major turnover event (“Grande Coupure”) at this time. Our results highlight the power and limitations of inferring diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species concepts.
    • Mixing genetically differentiated populations successfully boosts diversity of an endangered carnivore

      McLennan, E. A.; Grueber, Catherine E.; Wise, P.; Belov, K.; Hogg, Carolyn J. (2020)
      …We used an introduced population of Tasmanian devils Sarcophilus harrisii descended from two genetically differentiated source populations to illustrate the benefits of genetic admixture for translocation programmes. Devils are endangered due to an infectious cancer causing 80% population declines across their range since disease emergence in 1996…. As part of their conservation management, devils were introduced to Maria Island, Tasmania in an assisted colonization in 2012 with supplementations in 2013 and 2017….
    • Molecular phylogeny and evolution of the Perissodactyla

      Steiner, Cynthia C.; Ryder, Oliver A. (2011)
      The evolution of perissodactyls (rhinoceroses, tapirs, and horses) has been well studied primarily because of their extensive fossil record. Nevertheless, controversy persists regarding relationships of some of the extant taxa, reflecting inconsistencies between molecular and morphological studies. Here we examine the phylogenetic relationships of 16 living perissodactyl species by concatenating two mitochondrial and nine nuclear genes, and we estimate their divergence times using a relaxed Bayesian molecular clock approach....
    • Molecular variation and population structure in critically endangered Turks and Caicos Rock Iguanas: identifying intraspecific conservation units and revising subspecific taxonomy

      Welch, Mark E.; Colosimo, Giuliano; Pasachnik, Stesha A.; Malone, Catherine L.; Hilton, Jace; Long, June; Getz, Angela H.; Alberts, Allison C.; Gerber, Glenn P. (2017)
      For species living in naturally fragmented habitats, the identification of conservation units is particularly challenging. Turks and Caicos Rock Iguanas, Cyclura carinata, are endemic to the Turks and Caicos Islands (TCI)....
    • No evidence of inbreeding depression in a Tasmanian devil insurance population despite significant variation in inbreeding

      Gooley, Rebecca M.; Hogg, Carolyn J.; Belov, Katherine; Grueber, Catherine E. (2017)
      Inbreeding depression occurs when inbred individuals experience reduced fitness as a result of reduced genome-wide heterozygosity. The Tasmanian devil faces extinction due to a contagious cancer, devil facial tumour disease (DFTD). An insurance metapopulation was established in 2006 to ensure the survival of the species and to be used as a source population for re-wilding and genetic rescue. The emergence of DFTD and the rapid decline of wild devil populations have rendered the species at risk of inbreeding depression. We used 33 microsatellite loci to (1) reconstruct a pedigree for the insurance population and (2) estimate genome-wide heterozygosity for 200 individuals. Using heterozygosity-fitness correlations, we investigated the effect of heterozygosity on six diverse fitness measures (ulna length, asymmetry, weight-at-weaning, testes volume, reproductive success and survival). Despite statistically significant evidence of variation in individual inbreeding in this population, we found no associations between inbreeding and any of our six fitness measurements. We propose that the benign environment in captivity may decrease the intensity of inbreeding depression, relative to the stressful conditions in the wild. Future work will need to measure fitness of released animals to facilitate translation of this data to the broader conservation management of the species in its native range.
    • Patterns of genetic partitioning and gene flow in the endangered San Bernardino kangaroo rat (Dipodomys merriami parvus) and implications for conservation management

      Hendricks, Sarah; Navarro, Asako Y.; Wang, Thea B.; Wilder, Aryn P.; Ryder, Oliver A.; Shier, Debra M. (2020)
      ...We examined the genetic diversity, population structure, and phylogeography of this subspecies using partial mitochrondrial DNA sequencing and microsatellite genotyping. Our study indicates that currently, the three remaining populations seem to be highly fragmented....
    • Pedigree reconstruction using molecular data reveals an early warning sign of gene diversity loss in an island population of Tasmanian devils (Sarcophilus harrisii)

      McLennan, Elspeth A.; Gooley, Rebecca M.; Wise, Phil; Belov, Katherine; Hogg, Carolyn J.; Grueber, Catherine E. (2018)
      Tasmanian devils have experienced an 85% population decline since the emergence of an infectious cancer. In response, a captive insurance population was established in 2006 with a subpopulation later introduced onto Maria Island, Tasmania. We aimed to (1) examine the genetic parameters of the Maria Island population as a stand-alone site and within its broader metapopulation context, (2) assess the efficacy of assisted colonisations, and (3) inform future translocations. This study reconstructs the pedigree of 86 island-born devils using 31 polymorphic microsatellite loci. Combined molecular and pedigree analysis was used to monitor change in population genetic parameters in 4 years since colonisation. Molecular analysis alone revealed no significant change in genetic diversity, while DNA-reconstructed pedigree analysis revealed a statistically significant increase in inbreeding due to skewed founder representation. Pedigree modelling predicted that gene diversity would only be maintained above the threshold of 95% for a further 2 years, dropping to 77.1% after 40 years. Modelling alternative supplementation strategies revealed introducing eight new founders every 3 years will enable the population to retain 95% gene diversity until 2056, provided the translocated animals breed; to ensure this we recommend introducing ten new females every 3 years. We highlight the value of combining pedigree analyses with molecular data, from both a single-site and metapopulation viewpoint, for analysing changes in genetic parameters within populations of conservation concern. The importance of post-release genetic monitoring in an established population is emphasised, given how quickly inbreeding can accumulate and gene diversity be lost.