Establishment, persistence and the importance of longitudinal monitoring in multi‐source reintroductions

Incorporating genetic data into conservation programmes improves management outcomes, but the impact of different sample grouping methods on genetic diversity analyses is poorly understood. To this end, the multi‐source reintroduction of the eastern bettong Bettongia gaimardi was used as a long‐term case study to investigate how sampling regimes may affect common genetic metrics and hence management decisions. The dataset comprised 5307 SNPs sequenced across 263 individuals. Samples included 45 founders from five genetically distinct Tasmanian source regions, and 218 of their descendants captured during annual monitoring at Mulligan’s Flat Woodland Sanctuary (121 samples across eight generations) and Tidbinbilla Nature Reserve (97 samples across nine generations). The most management‐informative sampling regime was found to be generational cohorts, providing detailed long‐term trends in genetic diversity. When these generation‐specific trends were not investigated, recent changes in population genetics were masked, and it became apparent that management recommendations would be less appropriate. The results also illuminated the importance of considering establishment and persistence as separate phases of a multi‐source reintroduction. The establishment phase (useful for informing early adaptive management) should consist of no less than two generations and continue until admixture is achieved (admixture defined here as >80% of individuals possessing >60% of source genotypes, with no one source composing >70% of >20% individuals’ genotype) is achieved. This ensures that the persistence phase analyses of population trends remain minimally biased. Based on this case study, we recommend that emphasis be given to the value of generationally specific analyses, and that conservation programmes collect DNA samples throughout the establishment and persistence phases and avoid collecting genetic samples only when the analysis is imminent. We also recommend that population genetic analyses for multi‐source reintroductions consider whether admixture has been achieved when calculating descriptive genetic metrics.

[1]  A. Weeks,et al.  Unbiased population heterozygosity estimates from genome-wide sequence data , 2020, bioRxiv.

[2]  M. Geary,et al.  The importance of long-term genetic monitoring of reintroduced populations: inbreeding in the natterjack toad (Epidalea calamita) , 2020 .

[3]  J. Pemberton,et al.  Genetic architecture and lifetime dynamics of inbreeding depression in a wild mammal , 2020, Nature Communications.

[4]  J. Robalo,et al.  Time matters: genetic composition and evaluation of effective population size in temperate coastal fish species , 2020, PeerJ.

[5]  V. Trenkel,et al.  Estimating effective population size using RADseq: Effects of SNP selection and sample size , 2020, Ecology and evolution.

[6]  A. Wayne,et al.  Integrating population genetics in an adaptive management framework to inform management strategies , 2019, Biodiversity and Conservation.

[7]  S. Cunningham,et al.  A reintroduced ecosystem engineer provides a germination niche for native plant species , 2019, Biodiversity and Conservation.

[8]  W. J. Kennington,et al.  Population Genomics of Bettongia lesueur: Admixing Increases Genetic Diversity with no Evidence of Outbreeding Depression , 2019, Genes.

[9]  E. Bignal,et al.  Evaluating the efficacy of independent versus simultaneous management strategies to address ecological and genetic threats to population viability , 2019, Journal of Applied Ecology.

[10]  William G. Batson,et al.  Transition to density dependence in a reintroduced ecosystem engineer , 2019, Biodiversity and Conservation.

[11]  A. Wayne,et al.  Guidelines for genetic management in mammal translocation programs , 2019, Biological Conservation.

[12]  W. J. Kennington,et al.  Mixing Genetically and Morphologically Distinct Populations in Translocations: Asymmetrical Introgression in A Newly Established Population of the Boodie (Bettongia lesueur) , 2019, Genes.

[13]  P. Menkhorst,et al.  Lifetime Fitness Costs of Inbreeding and Being Inbred in a Critically Endangered Bird , 2019, Current Biology.

[14]  Ben C. Augustine,et al.  Early genetic outcomes of American black bear reintroductions in the Central Appalachians, USA , 2019, Ursus.

[15]  I. Gordon,et al.  Returning a lost process by reintroducing a locally extinct digging marsupial , 2019, PeerJ.

[16]  C. Battey,et al.  Minor allele frequency thresholds strongly affect population structure inference with genomic data sets , 2019, Molecular ecology resources.

[17]  P. Unmack,et al.  dartr: An r package to facilitate analysis of SNP data generated from reduced representation genome sequencing , 2018, Molecular ecology resources.

[18]  D. Díez-del-Molino,et al.  Quantifying Temporal Genomic Erosion in Endangered Species. , 2017, Trends in ecology & evolution.

[19]  L. Keller,et al.  Population genomics analyses of European ibex species show lower diversity and higher inbreeding in reintroduced populations , 2017, Evolutionary applications.

[20]  C. Cook,et al.  Aligning science and policy to achieve evolutionarily enlightened conservation , 2017, Conservation biology : the journal of the Society for Conservation Biology.

[21]  Jason G. Bragg,et al.  Genetic factors in threatened species recovery plans on three continents , 2016 .

[22]  Adrian D. Manning,et al.  REVIEW: Translocation tactics: a framework to support the IUCN Guidelines for wildlife translocations and improve the quality of applied methods , 2015 .

[23]  N. J. Ouborg,et al.  Genomics and the challenging translation into conservation practice. , 2015, Trends in ecology & evolution.

[24]  Ramesh Krishnan Ramasamy,et al.  STRUCTURE PLOT: a program for drawing elegant STRUCTURE bar plots in user friendly interface , 2014, SpringerPlus.

[25]  Omar De la Cruz,et al.  Population structure at different minor allele frequency levels , 2014, BMC Proceedings.

[26]  G. M. Macbeth,et al.  NeEstimator v2: re‐implementation of software for the estimation of contemporary effective population size (Ne) from genetic data , 2014, Molecular ecology resources.

[27]  A. Wayne,et al.  Genetic outcomes from the translocations of the critically endangered woylie , 2013 .

[28]  Rod Peakall,et al.  GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update , 2012, Bioinform..

[29]  A. Manning,et al.  The ‘making of’ the Mulligans Flat – Goorooyarroo experimental restoration project , 2012 .

[30]  D. Lindenmayer,et al.  An assessment of scientific approaches towards species relocations in Australia , 2012 .

[31]  Thibaut Jombart,et al.  adegenet 1.3-1: new tools for the analysis of genome-wide SNP data , 2011, Bioinform..

[32]  D. Lindenmayer,et al.  Integrating research and restoration: the establishment of a long-term woodland experiment in south-eastern Australia , 2011 .

[33]  R. Frankham,et al.  Assessing the benefits and risks of translocations in changing environments: a genetic perspective , 2011, Evolutionary applications.

[34]  Lisa J. Martin,et al.  The effect of minor allele frequency on the likelihood of obtaining false positives , 2009, BMC Proceedings.

[35]  R. Waples,et al.  Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution , 2009, Evolutionary Applications.

[36]  Christopher N. Johnson,et al.  Body mass and extinction risk in Australian marsupials: The ‘Critical Weight Range’ revisited , 2009 .

[37]  R. Waples,et al.  ldne: a program for estimating effective population size from data on linkage disequilibrium , 2008, Molecular ecology resources.

[38]  Thibaut Jombart,et al.  adegenet: a R package for the multivariate analysis of genetic markers , 2008, Bioinform..

[39]  Doug P Armstrong,et al.  Developing the Science of Reintroduction Biology , 2007, Conservation biology : the journal of the Society for Conservation Biology.

[40]  S. Edmands.  Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management , 2006, Molecular ecology.

[41]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[42]  R. Waples,et al.  A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci* , 2006, Conservation Genetics.

[43]  A. C. Sørensen,et al.  Inbreeding – lessons from animal breeding, evolutionary biology and conservation genetics , 2005 .

[44]  J. Goudet.  HIERFSTAT , a package for R to compute and test hierarchical F -statistics , 2005 .

[45]  R. Frankham.  Genetics and conservation biology. , 2003, Comptes rendus biologies.

[46]  L. Keller,et al.  Inbreeding effects in wild populations. , 2002 .

[47]  David B. Lindenmayer,et al.  An assessment of the published results of animal relocations , 2000 .

[48]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[49]  Jeff Short,et al.  The extinction of rat-kangaroos (Marsupialia:Potoroidae) in New South Wales, Australia , 1998 .

[50]  Graeme Caughley,et al.  Directions in conservation biology , 1994 .

[51]  Shirley A. Miller,et al.  A simple salting out procedure for extracting DNA from human nucleated cells. , 1988, Nucleic acids research.

[52]  R. Rose.  Reproductive biology of the Tasmanian Bettong (Bettongia gaimardi: Macropodidae) , 1987 .

[53]  S. Wright.  THE INTERPRETATION OF POPULATION STRUCTURE BY F‐STATISTICS WITH SPECIAL REGARD TO SYSTEMS OF MATING , 1965 .

[54]  T. De Meeûs,et al.  Revisiting FIS, FST, Wahlund Effects, and Null Alleles , 2018, The Journal of heredity.

[55]  S. Soorae.  Global Re-introduction Perspectives 2016 Case-studies from around the globe , 2016 .

[56]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[57]  A. Kilian,et al.  Diversity arrays technology: a generic genome profiling technology on open platforms. , 2012, Methods in molecular biology.

[58]  P. Seddon,et al.  Directions in reintroduction biology. , 2008, Trends in ecology & evolution.

[59]  N. L. McKenzie,et al.  Patterns in the modern decline of western Australia's vertebrate fauna: Causes and conservation implications , 1989 .

[60]  H. Fineberg,et al.  Evaluating efficacy. , 1980, AJR. American journal of roentgenology.