Publications by authors named "Robert Lacy"

34 Publications

Applying the zoo model to conservation of threatened exceptional plant species.

Conserv Biol 2020 12 17;34(6):1416-1425. Epub 2020 Jun 17.

Negaunee Institute for Plant Conservation Science and Action, Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, IL, 60022, U.S.A.

Maintaining a living plant collection is the most common method of ex situ conservation for plant species that cannot be seed banked (i.e., exceptional species). Viability of living collections, and their value for future conservation efforts, can be limited without coordinated efforts to track and manage individuals across institutions. Using a pedigree-focused approach, the zoological community has established an inter-institutional infrastructure to support long-term viability of captive animal populations. We assessed the ability of this coordinated metacollection infrastructure to support the conservation of 4 plant species curated in living collections at multiple botanic gardens around the world. Limitations in current practices include the inability to compile, share, and analyze plant collections data at the individual level, as well as difficulty in tracking original provenance of ex situ material. The coordinated metacollection framework used by zoos can be adopted by the botanical community to improve conservation outcomes by minimizing the loss of genetic diversity in collections. We suggest actions to improve ex situ conservation of exceptional plant species, including developing a central database to aggregate data and track unique individuals of priority threatened species among institutions and adapting a pedigree-based population management tool that incorporates life-history aspects unique to plants. If approached collaboratively across regional, national, and global scales, these actions could transform ex situ conservation of threatened plant species.
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http://dx.doi.org/10.1111/cobi.13503DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7754355PMC
December 2020

Demographic reconstruction from ancient DNA supports rapid extinction of the great auk.

Elife 2019 11 26;8. Epub 2019 Nov 26.

Department of Anatomy, University of Otago, Dunedin, New Zealand.

The great auk was once abundant and distributed across the North Atlantic. It is now extinct, having been heavily exploited for its eggs, meat, and feathers. We investigated the impact of human hunting on its demise by integrating genetic data, GPS-based ocean current data, and analyses of population viability. We sequenced complete mitochondrial genomes of 41 individuals from across the species' geographic range and reconstructed population structure and population dynamics throughout the Holocene. Taken together, our data do not provide any evidence that great auks were at risk of extinction prior to the onset of intensive human hunting in the early 16 century. In addition, our population viability analyses reveal that even if the great auk had not been under threat by environmental change, human hunting alone could have been sufficient to cause its extinction. Our results emphasise the vulnerability of even abundant and widespread species to intense and localised exploitation.
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http://dx.doi.org/10.7554/eLife.47509DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6879203PMC
November 2019

Biological and Sociopolitical Sources of Uncertainty in Population Viability Analysis for Endangered Species Recovery Planning.

Sci Rep 2019 07 12;9(1):10130. Epub 2019 Jul 12.

Turner Endangered Species Fund, 901 Technology Blvd, Bozeman, Montana, 59718, USA.

Although population viability analysis (PVA) can be an important tool for strengthening endangered species recovery efforts, the extent to which such analyses remain embedded in the social process of recovery planning is often unrecognized. We analyzed two recovery plans for the Mexican wolf that were developed using similar data and methods but arrived at contrasting conclusions as to appropriate recovery goals or criteria. We found that approximately half of the contrast arose from uncertainty regarding biological data, with the remainder divided between policy-related decisions and mixed biological-policy factors. Contrasts arose from both differences in input parameter values and how parameter uncertainty informed the level of precaution embodied in resulting criteria. Policy-related uncertainty originated from contrasts in thresholds for acceptable risk and disagreement as to how to define endangered species recovery. Rather than turning to PVA to produce politically acceptable definitions of recovery that appear science-based, agencies should clarify the nexus between science and policy elements in their decision processes. The limitations we identify in endangered-species policy and how PVAs are conducted as part of recovery planning must be addressed if PVAs are to fulfill their potential to increase the odds of successful conservation outcomes.
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http://dx.doi.org/10.1038/s41598-019-45032-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6626004PMC
July 2019

Conservation and Genetics.

Yale J Biol Med 2018 12 21;91(4):491-501. Epub 2018 Dec 21.

Monash University, Clayton, Victoria, Australia.

Humans are responsible for a cataclysm of species extinction that will change the world as we see it, and will adversely affect human health and wellbeing. We need to understand at individual and societal levels why species conservation is important. Accepting the premise that species have value, we need to next consider the mechanisms underlying species extinction and what we can do to reverse the process. One of the last stages of species extinction is the reduction of a species to a few populations of relatively few individuals, a scenario that leads invariably to inbreeding and its adverse consequences, inbreeding depression. Inbreeding depression can be so severe that populations become at risk of extinction not only because of the expression of harmful recessive alleles (alleles having no phenotypic effect when in the heterozygous condition, ., Aa, where is the recessive allele), but also because of their inability to respond genetically with sufficient speed to adapt to changing environmental conditions. However, new conservation approaches based on foundational quantitative and population genetic theory advocate for active genetic management of fragmented populations by facilitating gene movements between populations, ., admixture, or genetic rescue. Why species conservation is critical, the genetic consequences of small population size that often lead to extinction, and possible solutions to the problem of small population size are discussed and presented.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6302618PMC
December 2018

Lessons from 30 years of population viability analysis of wildlife populations.

Authors:
Robert C Lacy

Zoo Biol 2019 Jan 26;38(1):67-77. Epub 2018 Dec 26.

Chicago Zoological Society, Brookfield, Illinois.

Population viability analysis (PVA) has been used for three decades to assess threats and evaluate conservation options for wildlife populations. What has been learned from PVA on in situ populations are valuable lessons also for assessing and managing viability and sustainability of ex situ populations. The dynamics of individual populations are unpredictable, due to limited knowledge about important factors, variability in the environment, and the probabilistic nature of demographic events. PVA considers such uncertainty within simulations that generate the distribution of likely fates for a population; management of ex situ populations should also take into consideration the uncertainty in our data and in the trajectories of populations. The processes affecting wildlife populations interact, with feedbacks often leading to amplified threats to viability; projections of ex situ populations should include such feedbacks to allow for management that foresees and responds to the cumulative and synergistic threats. PVA is useful for evaluating conservation options only if the goals for each population and measures of success are first clearly identified; similarly, for ex situ populations to contribute maximally to species conservation, the purposes for the population and definitions of sustainability in terms of acceptable risk must be documented. PVA requires a lot of data, knowledge of many processes affecting the populations, modeling expertize, and understanding of management goals and constraints. Therefore, to be useful in guiding conservation it must be a collaborative, trans-disciplinary, and social process. PVA can help integrate management of in situ and ex situ populations within comprehensive species conservation plans.
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http://dx.doi.org/10.1002/zoo.21468DOI Listing
January 2019

Evaluating anthropogenic threats to endangered killer whales to inform effective recovery plans.

Sci Rep 2017 10 26;7(1):14119. Epub 2017 Oct 26.

Raincoast Conservation Foundation, Sidney, BC V8L 3Y3, Canada.

Understanding cumulative effects of multiple threats is key to guiding effective management to conserve endangered species. The critically endangered, Southern Resident killer whale population of the northeastern Pacific Ocean provides a data-rich case to explore anthropogenic threats on population viability. Primary threats include: limitation of preferred prey, Chinook salmon; anthropogenic noise and disturbance, which reduce foraging efficiency; and high levels of stored contaminants, including PCBs. We constructed a population viability analysis to explore possible demographic trajectories and the relative importance of anthropogenic stressors. The population is fragile, with no growth projected under current conditions, and decline expected if new or increased threats are imposed. Improvements in fecundity and calf survival are needed to reach a conservation objective of 2.3% annual population growth. Prey limitation is the most important factor affecting population growth. However, to meet recovery targets through prey management alone, Chinook abundance would have to be sustained near the highest levels since the 1970s. The most optimistic mitigation of noise and contaminants would make the difference between a declining and increasing population, but would be insufficient to reach recovery targets. Reducing acoustic disturbance by 50% combined with increasing Chinook by 15% would allow the population to reach 2.3% growth.
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http://dx.doi.org/10.1038/s41598-017-14471-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5658391PMC
October 2017

A father effect explains sex-ratio bias.

Proc Biol Sci 2017 Aug;284(1861)

Chicago Zoological Society, Brookfield, IL, USA.

Sex ratio allocation has important fitness consequences, and theory predicts that parents should adjust offspring sex ratio in cases where the fitness returns of producing male and female offspring vary. The ability of fathers to bias offspring sex ratios has traditionally been dismissed given the expectation of an equal proportion of X- and Y-chromosome-bearing sperm (CBS) in ejaculates due to segregation of sex chromosomes at meiosis. This expectation has been recently refuted. Here we used to demonstrate that sex ratio is explained by an exclusive effect of the father, and suggest a likely mechanism by which male-driven sex-ratio bias is attained. We identified a male sperm morphological marker that is associated with the mechanism leading to sex ratio bias; differences among males in the sperm nucleus area (a proxy for the sex chromosome that the sperm contains) explain 22% variation in litter sex ratio. We further show the role played by the sperm nucleus area as a mediator in the relationship between individual genetic variation and sex-ratio bias. Fathers with high levels of genetic variation had ejaculates with a higher proportion of sperm with small nuclei area. This, in turn, led to siring a higher proportion of sons (25% increase in sons per 0.1 decrease in the inbreeding coefficient). Our results reveal a plausible mechanism underlying unexplored male-driven sex-ratio biases. We also discuss why this pattern of paternal bias can be adaptive. This research puts to rest the idea that father contribution to sex ratio variation should be disregarded in vertebrates, and will stimulate research on evolutionary constraints to sex ratios-for example, whether fathers and mothers have divergent, coinciding, or neutral sex allocation interests. Finally, these results offer a potential explanation for those intriguing cases in which there are sex ratio biases, such as in humans.
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http://dx.doi.org/10.1098/rspb.2017.1159DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5577485PMC
August 2017

Inbreeding and selection shape genomic diversity in captive populations: Implications for the conservation of endangered species.

PLoS One 2017 19;12(4):e0175996. Epub 2017 Apr 19.

Department of Forestry and Natural Resources, Purdue University, West Lafayette, Indiana, United States of America.

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.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0175996PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5396937PMC
April 2017

What to do when we can't bank on seeds: What botanic gardens can learn from the zoo community about conserving plants in living collections.

Am J Bot 2016 09 30;103(9):1541-3. Epub 2016 Aug 30.

Botanic Gardens Conservation International, 199 Kew Road, Richmond, Surrey TW9 3BW UK.

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http://dx.doi.org/10.3732/ajb.1600247DOI Listing
September 2016

Use of animals with partially known ancestries in scientifically managed breeding programs.

Zoo Biol 2016 Jul 27;35(4):319-25. Epub 2016 May 27.

Chicago Zoological Society, Conservation Science, Brookfield, Illinois.

Animals with only partially known ancestry present a problem for population managers because it can be difficult to determine their relative genetic value to the population. So long as their ancestry is not completely unknown, population management software such as PMx can calculate a mean kinship for these animals, but that mean kinship is calculated such that there is no decrease in relative genetic value or "penalty" for only partially known ancestry. However, there is a longer-term genetic cost to having animals with only partially known ancestry in the population, and thus it is appropriate to "penalize" animals with partially known ancestry to some extent. The challenge is determining the correct "penalty" which will serve to decrease the percent unknown ancestry in subsequent generations while not causing excessive selection against the known ancestry of the animal. A new parameter of relative genetic value is developed which takes into account both an animal's mean kinship as well as its percent known ancestry. The method used in PMx to calculate the mean kinships also in general overestimates the inbreeding coefficients of offspring of animals with partially known ancestry when the known parents share a common ancestor, but can underestimate inbreeding if common ancestors exist within the unknown portion of the pedigree. This may result in population managers selecting less suitable pairs for breeding in an attempt to avoid an apparent higher level of inbreeding. A parameter is developed that adjusts the inbreeding coefficient to more accurately reflect the likely inbreeding coefficient of potential offspring. Zoo Biol. 35:319-325, 2016. © 2016 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/zoo.21295DOI Listing
July 2016

Pedigree analysis for the genetic management of group-living species.

Ecol Evol 2016 05 2;6(10):3067-78. Epub 2016 Apr 2.

Chicago Zoological Society Brookfield Illinois 60513.

Captive breeding programs are an important tool for the conservation of endangered species. These programs are commonly managed using pedigrees containing information about the history of each individual's family, such as breeding pairs and parentage. However, there are some species that are kept in groups where it is hard to distinguish between particular individuals within the group, making it very difficult to record any information at an individual level. Currently, software and methods commonly used for registering and analyzing pedigrees to help manage populations at an individual level are not adequate for managing these group-living species. Therefore, there is a need to further develop these tools and methodologies for pedigree analysis to better manage group-living species. PMx is a program used for the management of ex situ populations in zoos and aquariums. We adapted the pedigree analysis method implemented in PMx to analyze pedigrees (records of descendant lineages) of group-living species. In addition, we developed a group pedigree data entry sheet and group2PMx, a converter program that enables group datasets to be imported into PMx. We show how pedigree analysis of a group-living species can be used for population management using the studbook of the endangered Texas blind cave salamander Eurycea rathbuni. Such analyses of the pedigree of groups can improve the management of group-living species in ex situ breeding programs. Firstly, it enables better management decisions based on more accurate genetic measures between groups, allowing for greater control of inbreeding. Secondly, it can improve the conditions in which group-living species are held by adapting husbandry practices to better reflect conditions of these species living in the wild. The use of the spreadsheet and group2PMx extends the application of PMx, allowing conservation managers and other institutions outside the zoo and aquarium community to easily import and analyze their pedigree data.
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http://dx.doi.org/10.1002/ece3.1831DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4821840PMC
May 2016

The relative importance of reproduction and survival for the conservation of two dolphin populations.

Ecol Evol 2016 06 20;6(11):3496-3512. Epub 2016 Apr 20.

Evolution and Ecology Research Centre School of Biological, Earth and Environmental Sciences University of New South Wales Sydney New South Wales 2052 Australia.

It has been proposed that in slow-growing vertebrate populations survival generally has a greater influence on population growth than reproduction. Despite many studies cautioning against such generalizations for conservation, wildlife management for slow-growing populations still often focuses on perturbing survival without careful evaluation as to whether those changes are likely or feasible. Here, we evaluate the relative importance of reproduction and survival for the conservation of two bottlenose dolphin ( cf ) populations: a large, apparently stable population and a smaller one that is forecast to decline. We also assessed the feasibility and effectiveness of wildlife management objectives aimed at boosting either reproduction or survival. Consistent with other analytically based elasticity studies, survival had the greatest effect on population trajectories when altering vital rates by equal proportions. However, the findings of our alternative analytical approaches are in stark contrast to commonly used proportional sensitivity analyses and suggest that reproduction is considerably more important. We show that in the stable population reproductive output is higher, and adult survival is lower;the difference in viability between the two populations is due to the difference in reproduction;reproductive rates are variable, whereas survival rates are relatively constant over time;perturbations on the basis of observed, temporal variation indicate that population dynamics are much more influenced by reproduction than by adult survival;for the apparently declining population, raising reproductive rates would be an effective and feasible tool to reverse the forecast population decline; increasing survival would be ineffective. Our findings highlight the importance of reproduction - even in slow-growing populations - and the need to assess the effect of natural variation in vital rates on population viability. We echo others in cautioning against generalizations based on life-history traits and recommend that population modeling for conservation should also take into account the magnitude of vital rate changes that could be attained under alternative management scenarios.
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http://dx.doi.org/10.1002/ece3.2130DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513288PMC
June 2016

Cloning and molecular characterization of telomerase reverse transcriptase (TERT) and telomere length analysis of Peromyscus leucopus.

Gene 2015 Aug 9;568(1):8-18. Epub 2015 May 9.

Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD, USA.

Telomerase reverse transcriptase (TERT) is the catalytic subunit of telomerase complex that regulates telomerase activity to maintain telomere length for all animals with linear chromosomes. As the Mus musculus (MM) laboratory mouse has very long telomeres compared to humans, a potential alternative animal model for telomere research is the Peromyscus leucopus (PL) mouse that has telomere lengths close to the human range and has the wild counterparts for comparison. We report the full TERT coding sequence (pTERT) from PL mice to use in the telomere research. Comparative analysis with eight other mammalian TERTs revealed a pTERT protein considerably homologous to other TERTs and preserved all TERT specific-sequence signatures, yet with some distinctive features. pTERT displayed the highest nucleotide and amino acid sequence homology with hamster TERT. Unlike human but similar to MM mice, pTERT expression was detected in various adult somatic tissues of PL mice, with the highest expression in testes. Four different captive stocks of PL mice and wild-captured PL mice each displayed group-specific average telomere lengths, with the longest and shortest telomeres in inbred and outbred stock mice, respectively. pTERT showed considerable numbers of synonymous and nonsynonymous mutations. A pTERT proximal promoter region cloned was homologous among PL and MM mice and rat, but with species-specific features. From PL mice, we further cloned and characterized ribosomal protein, large, P0 (pRPLP0) to use as an internal control for various assays. Peromyscus mice have been extensively used for various studies, including human diseases, for which pTERT and pRPLP0 would be useful tools.
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http://dx.doi.org/10.1016/j.gene.2015.05.013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470739PMC
August 2015

Timing and severity of immunizing diseases in rabbits is controlled by seasonal matching of host and pathogen dynamics.

J R Soc Interface 2015 Feb;12(103)

The Environment Institute and School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia.

Infectious diseases can exert a strong influence on the dynamics of host populations, but it remains unclear why such disease-mediated control only occurs under particular environmental conditions. We used 16 years of detailed field data on invasive European rabbits (Oryctolagus cuniculus) in Australia, linked to individual-based stochastic models and Bayesian approximations, to test whether (i) mortality associated with rabbit haemorrhagic disease (RHD) is driven primarily by seasonal matches/mismatches between demographic rates and epidemiological dynamics and (ii) delayed infection (arising from insusceptibility and maternal antibodies in juveniles) are important factors in determining disease severity and local population persistence of rabbits. We found that both the timing of reproduction and exposure to viruses drove recurrent seasonal epidemics of RHD. Protection conferred by insusceptibility and maternal antibodies controlled seasonal disease outbreaks by delaying infection; this could have also allowed escape from disease. The persistence of local populations was a stochastic outcome of recovery rates from both RHD and myxomatosis. If susceptibility to RHD is delayed, myxomatosis will have a pronounced effect on population extirpation when the two viruses coexist. This has important implications for wildlife management, because it is likely that such seasonal interplay and disease dynamics has a strong effect on long-term population viability for many species.
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http://dx.doi.org/10.1098/rsif.2014.1184DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4305421PMC
February 2015

Measuring relatedness between inbred individuals.

J Hered 2015 Jan-Feb;106(1):20-5. Epub 2014 Dec 2.

School of Life Sciences, Arizona State University, Tempe, AZ 85287 (Hedrick); and Chicago Zoological Society, Brookfield, IL 60513 (Lacy).

Genetic relatedness between individuals is an important measure in many areas of biology. However, some relatedness measures for use with molecular (allele) data assume that the individuals themselves are not inbred. Here, we present a new measure of relatedness based on the different modes of identity-by-descent for alleles that has an upper bound of 1 even when the individuals being compared are themselves inbred. This new measure is compared to several other measures of relatedness using several simple examples and pedigree data from the wolf population in Isle Royale National Park.
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http://dx.doi.org/10.1093/jhered/esu072DOI Listing
July 2015

The impacts of inbreeding, drift and selection on genetic diversity in captive breeding populations.

Mol Ecol 2015 Jan 31;24(1):98-110. Epub 2014 Dec 31.

Department of Forestry and Natural Resources, Purdue University, 715 W. State St., West Lafayette, IN, 47906, USA.

The goal of captive breeding programmes is often to maintain genetic diversity until re-introductions can occur. However, due in part to changes that occur in captive populations, approximately one-third of re-introductions fail. We evaluated genetic changes in captive populations using microsatellites and mtDNA. We analysed six populations of white-footed mice that were propagated for 20 generations using two replicates of three protocols: random mating (RAN), minimizing mean kinship (MK) and selection for docility (DOC). We found that MK resulted in the slowest loss of microsatellite genetic diversity compared to RAN and DOC. However, the loss of mtDNA haplotypes was not consistent among replicate lines. We compared our empirical data to simulated data and found no evidence of selection. Our results suggest that although the effects of drift may not be fully mitigated, MK reduces the loss of alleles due to inbreeding more effectively than random mating or docility selection. Therefore, MK should be preferred for captive breeding. Furthermore, our simulations show that incorporating microsatellite data into the MK framework reduced the magnitude of drift, which may have applications in long-term or extremely genetically depauperate captive populations.
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http://dx.doi.org/10.1111/mec.13020DOI Listing
January 2015

High-throughput sequencing reveals inbreeding depression in a natural population.

Proc Natl Acad Sci U S A 2014 Mar 28;111(10):3775-80. Epub 2014 Feb 28.

Department of Animal Behaviour, Bielefeld University, 33501 Bielefeld, Germany.

Proxy measures of genome-wide heterozygosity based on approximately 10 microsatellites have been used to uncover heterozygosity fitness correlations (HFCs) for a wealth of important fitness traits in natural populations. However, effect sizes are typically very small and the underlying mechanisms remain contentious, as a handful of markers usually provides little power to detect inbreeding. We therefore used restriction site associated DNA (RAD) sequencing to accurately estimate genome-wide heterozygosity, an approach transferrable to any organism. As a proof of concept, we first RAD sequenced oldfield mice (Peromyscus polionotus) from a known pedigree, finding strong concordance between the inbreeding coefficient and heterozygosity measured at 13,198 single-nucleotide polymorphisms (SNPs). When applied to a natural population of harbor seals (Phoca vitulina), a weak HFC for parasite infection based on 27 microsatellites strengthened considerably with 14,585 SNPs, the deviance explained by heterozygosity increasing almost fivefold to a remarkable 49%. These findings arguably provide the strongest evidence to date of an HFC being due to inbreeding depression in a natural population lacking a pedigree. They also suggest that under some circumstances heterozygosity may explain far more variation in fitness than previously envisaged.
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http://dx.doi.org/10.1073/pnas.1318945111DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3956162PMC
March 2014

Metamodels for transdisciplinary analysis of wildlife population dynamics.

PLoS One 2013 13;8(12):e84211. Epub 2013 Dec 13.

Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia, United States of America.

Wildlife population models have been criticized for their narrow disciplinary perspective when analyzing complexity in coupled biological - physical - human systems. We describe a "metamodel" approach to species risk assessment when diverse threats act at different spatiotemporal scales, interact in non-linear ways, and are addressed by distinct disciplines. A metamodel links discrete, individual models that depict components of a complex system, governing the flow of information among models and the sequence of simulated events. Each model simulates processes specific to its disciplinary realm while being informed of changes in other metamodel components by accessing common descriptors of the system, populations, and individuals. Interactions among models are revealed as emergent properties of the system. We introduce a new metamodel platform, both to further explain key elements of the metamodel approach and as an example that we hope will facilitate the development of other platforms for implementing metamodels in population biology, species risk assessments, and conservation planning. We present two examples - one exploring the interactions of dispersal in metapopulations and the spread of infectious disease, the other examining predator-prey dynamics - to illustrate how metamodels can reveal complex processes and unexpected patterns when population dynamics are linked to additional extrinsic factors. Metamodels provide a flexible, extensible method for expanding population viability analyses beyond models of isolated population demographics into more complete representations of the external and intrinsic threats that must be understood and managed for species conservation.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0084211PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3862810PMC
September 2014

Developing metapopulation connectivity criteria from genetic and habitat data to recover the endangered Mexican wolf.

Conserv Biol 2014 Feb 20;28(1):76-86. Epub 2013 Sep 20.

Klamath Center for Conservation Research, P.O. Box 104, Orleans, CA, 95556, U.S.A..

Restoring connectivity between fragmented populations is an important tool for alleviating genetic threats to endangered species. Yet recovery plans typically lack quantitative criteria for ensuring such population connectivity. We demonstrate how models that integrate habitat, genetic, and demographic data can be used to develop connectivity criteria for the endangered Mexican wolf (Canis lupus baileyi), which is currently being restored to the wild from a captive population descended from 7 founders. We used population viability analysis that incorporated pedigree data to evaluate the relation between connectivity and persistence for a restored Mexican wolf metapopulation of 3 populations of equal size. Decreasing dispersal rates greatly increased extinction risk for small populations (<150-200), especially as dispersal rates dropped below 0.5 genetically effective migrants per generation. We compared observed migration rates in the Northern Rocky Mountains (NRM) wolf metapopulation to 2 habitat-based effective distance metrics, least-cost and resistance distance. We then used effective distance between potential primary core populations in a restored Mexican wolf metapopulation to evaluate potential dispersal rates. Although potential connectivity was lower in the Mexican wolf versus the NRM wolf metapopulation, a connectivity rate of >0.5 genetically effective migrants per generation may be achievable via natural dispersal under current landscape conditions. When sufficient data are available, these methods allow planners to move beyond general aspirational connectivity goals or rules of thumb to develop objective and measurable connectivity criteria that more effectively support species recovery. The shift from simple connectivity rules of thumb to species-specific analyses parallels the previous shift from general minimum-viable-population thresholds to detailed viability modeling in endangered species recovery planning.
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http://dx.doi.org/10.1111/cobi.12156DOI Listing
February 2014

Evolution of Peromyscus leucopus mice in response to a captive environment.

PLoS One 2013 6;8(8):e72452. Epub 2013 Aug 6.

Chicago Zoological Society, Brookfield, Illinois, United States of America.

Many wildlife species are propagated in captivity as models for behavioral, physiological, and genetic research or to provide assurance populations to protect threatened species. However, very little is known about how animals evolve in the novel environment of captivity. The histories of most laboratory strains are poorly documented, and protected populations of wildlife species are usually too small and too short-term to allow robust statistical analysis. To document the evolutionary change in captive breeding programs, we monitored reproduction and behavior across 18 generations in six experimental populations of Peromyscusleucopus mice started from a common set of 20 wild-caught founders. The mice were propagated under three breeding protocols: a strategy to retain maximal genetic diversity, artificial selection against stereotypic behaviors that were hypothesized to reflect poor adaptation to captivity, and random bred controls. Two replicates were maintained with each protocol, and inter-replicate crosses at generations 19 and 20 were used to reverse accumulated inbreeding. We found that one of the stereotypic behaviors (repetitive flipping) was positively associated with reproductive fitness, while the other (gnawing) was relatively invariant. Selection to reduce these stereotypic behaviors caused marked reduction in reproduction, and populations not under artificial selection to reduce these behaviors responded with large increases in flipping. In non-selected populations, there was rapid evolution toward much higher proportion of pairs breeding and more rapid conception. Litter size, pup survival, and weaning mass all declined slowly, to the extent that would be predicted based on inbreeding depression. Inter-crossing between replicate populations reversed these declines in fitness components but did not reverse the changes in behavior or the accelerated breeding. These findings indicate that adaptation to captivity can be rapid, affecting reproductive patterns and behaviors, even under breeding protocols designed to minimize the rate of genetic change due to random drift and inadvertent selection.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0072452PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3735520PMC
April 2014

No need for disease: testing extinction hypotheses for the thylacine using multi-species metamodels.

J Anim Ecol 2013 Mar 24;82(2):355-64. Epub 2013 Jan 24.

Environment Institute and School of Earth and Environmental Science, University of Adelaide, Adelaide, SA, 5005, Australia.

Population viability analysis (PVA) is widely used to assess the extinction risk of threatened species and to evaluate different management strategies. However, conventional PVA neglects important biotic interactions and therefore can fail to identify important threatening processes. We designed a new PVA approach that includes species interactions explicitly by networking species models within a single 'metamodel'. We demonstrate the utility of PVA metamodels by employing them to reinterpret the extinction of the carnivorous, marsupial thylacine Thylacinus cynocephalus in Tasmania. In particular, we test the claim that well-documented impacts of European settlement cannot account for this extinction and that an unknown disease must have been an additional and necessary cause. We first constructed a classical, single-species PVA model for thylacines, which was then extended by incorporation within a dynamic predator-herbivore-vegetation metamodel that accounted for the influence of Europeans on the thylacine's prey base. Given obvious parameter uncertainties, we explored both modelling approaches with rigorous sensitivity analyses. Single-species PVA models were unable to recreate the thylacine's extinction unless a high human harvest, small starting population size or low maximum population growth rate was assumed, even if disease effects were included from 1906 to 1909. In contrast, we readily recreated the thylacine's demise using disease-free multi-species metamodels that simulated declines in native prey populations (particularly due to competition with introduced sheep). Dynamic, multi-species metamodels provide a simple, flexible framework for studying current species declines and historical extinctions caused by complex, interacting factors.
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http://dx.doi.org/10.1111/1365-2656.12029DOI Listing
March 2013

Effects of inbreeding on skeletal size and fluctuating asymmetry of Peromyscus polionotus mice.

Zoo Biol 2013 Mar 19;32(2):125-33. Epub 2012 Jul 19.

Department of Conservation Science, Chicago Zoological Society, Brookfield, Illinois 60513, USA.

Measurements of size and asymmetry in morphology might provide early indications of damaging effects of inbreeding or other genetic changes in conservation breeding programs. We examined the effects of inbreeding on size and fluctuating asymmetry (FA) in skull and limb bone measurements in experimental populations of three subspecies of Peromyscus polionotus mice that had previously been shown to suffer significant reductions in reproductive success when inbred. Inbreeding caused significant depression in mean size in two of the subspecies (P. p. rhoadsi and P. p. subgriseus), but the effects were smaller in the third (P. p. leucocephalus). Inbreeding caused an increase in FA of just one of eight bilateral traits in one subspecies (P. p. rhoadsi). Inbreeding depression in size was more easily detected than the effects of inbreeding on FA. FA may be much less sensitive to inbreeding and other stresses than are more direct measures of fitness such as reproductive output and body mass growth rate. Given the large sample sizes and statistical complexity required to assess changes to typically very small levels of FA in captive populations, FA will not likely provide a useful measure of inbreeding depression in captive populations.
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http://dx.doi.org/10.1002/zoo.21035DOI Listing
March 2013

Achieving true sustainability of zoo populations.

Authors:
Robert C Lacy

Zoo Biol 2013 Jan-Feb;32(1):19-26. Epub 2012 Jul 2.

Chicago Zoological Society, Brookfield, Illinois, USA.

For the last 30 years, cooperative management of irreplaceable animal populations in zoos and aquariums has focused primarily on the goal of minimizing genetic decay within defined time frames, and large advances have been made in technologies to optimize genetic management of closed populations. However, recent analyses have shown that most zoo programs are not projected to meet their stated goals. This has been described as a lack of achieving "sustainability" of the populations, yet by definition a goal of managed decay is not a plan for sustainability. True sustainability requires management of the resource in manner that does not deplete its value for the future. Achieving such sustainability for many managed populations may require changing from managing isolated populations to managing populations that are part of a broader metapopulation, with carefully considered exchange between populations across a spectrum of ex situ to in situ. Managing zoo populations as components of comprehensive conservation strategies for the species will require research on determinants of various kinds of genetic, physiological, behavioral, and morphological variation and their roles in population viability, development of an array of management techniques and tools, training of population managers in metapopulation management and integrated conservation planning, and projections of impacts of management strategies on the viability of the captive populations and all populations that are interactively managed or affected. Such a shift in goals and methods would result in zoo population management being an ongoing part of species conservation rather than short-term or isolated from species conservation. Zoo Biol. 32:19-26, 2013. © 2012 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/zoo.21029DOI Listing
July 2013

Extending pedigree analysis for uncertain parentage and diverse breeding systems.

Authors:
Robert C Lacy

J Hered 2012 Mar-Apr;103(2):197-205. Epub 2012 Jan 24.

Department of Conservation Science, Chicago Zoological Society, Brookfield, IL 60513, USA.

Breeding programs aimed at conserving genetic diversity in populations of wildlife or rare domestic breeds rely on detailed pedigree analysis for selection of breeders that will minimize the loss of alleles, reduce the accumulation of inbreeding, and maintain gene diversity. Commonly, techniques use a matrix of kinship coefficients to derive measures of genetic variation, inbreeding, and the value of individuals as breeders. Although these techniques were first developed for use on known pedigrees of diploid individuals, the concepts and methods can be extended to apply to any entity that contains genes derived from definable sources (e.g., individual parents, social groups, colonies, gene banks) via a definable mechanism of heredity (e.g., sexual reproduction between separate sexes, hermaphroditic selfing, autozygous production of homozygous or haploid offspring, cloning). Individuals with partly unknown ancestry or multiple possible parents can also be incorporated into kinship calculations, based on probabilistic assignment of parental contributions. This paper presents the algorithms used in new PMx software to extend traditional pedigree analysis techniques used for complete pedigrees of sexually reproducing, diploid species to deal with missing information due to unknown or uncertain parentage, and other breeding systems such as clones, selfing hermaphrodites, and haploid offspring or autogamy.
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http://dx.doi.org/10.1093/jhered/esr135DOI Listing
June 2012

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

J Hered 2012 Mar-Apr;103(2):186-96. Epub 2012 Jan 12.

Department of Life Sciences, San Diego Zoo Global, San Diego, CA 92112-0551, USA.

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. We used a series of computer simulations to test 4 methods of minimizing average kinship across a variety of scenarios with varying generation lengths, mortality rates, reproductive rates, and rates of breeding pair success. "Static MK Selection" and "Dynamic MK Selection" are 2 methods for iteratively selecting genetically underrepresented individuals for breeding, whereas "Ranked MK Selection" and "Simultaneous MK Selection" are 2 methods for concurrently selecting the group of breeding individuals that produce offspring with the lowest average kinship. For populations with discrete generations (24 tested scenarios), we found that the Simultaneous and Ranked MK Selection methods were generally the best, nearly equivalent methods for selecting breeding pairs that retained GD and limited inbreeding. For populations with overlapping generations (198 tested scenarios), we found that Dynamic MK Selection was the most robust method for selecting breeding pairs. We used these results to provide guidelines for identifying which method of minimizing average kinship was most appropriate for various breeding program scenarios.
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http://dx.doi.org/10.1093/jhered/esr129DOI Listing
June 2012

Predicting the probability of outbreeding depression.

Conserv Biol 2011 Jun 12;25(3):465-75. Epub 2011 Apr 12.

Department of Biological Sciences, Macquarie University, NSW 2109, Australia.

Fragmentation of animal and plant populations typically leads to genetic erosion and increased probability of extirpation. Although these effects can usually be reversed by re-establishing gene flow between population fragments, managers sometimes fail to do so due to fears of outbreeding depression (OD). Rapid development of OD is due primarily to adaptive differentiation from selection or fixation of chromosomal variants. Fixed chromosomal variants can be detected empirically. We used an extended form of the breeders' equation to predict the probability of OD due to adaptive differentiation between recently isolated population fragments as a function of intensity of selection, genetic diversity, effective population sizes, and generations of isolation. Empirical data indicated that populations in similar environments had not developed OD even after thousands of generations of isolation. To predict the probability of OD, we developed a decision tree that was based on the four variables from the breeders' equation, taxonomic status, and gene flow within the last 500 years. The predicted probability of OD in crosses between two populations is elevated when the populations have at least one of the following characteristics: are distinct species, have fixed chromosomal differences, exchanged no genes in the last 500 years, or inhabit different environments. Conversely, the predicted probability of OD in crosses between two populations of the same species is low for populations with the same karyotype, isolated for <500 years, and that occupy similar environments. In the former case, we recommend crossing be avoided or tried on a limited, experimental basis. In the latter case, crossing can be carried out with low probability of OD. We used crosses with known results to test the decision tree and found that it correctly identified cases where OD occurred. Current concerns about OD in recently fragmented populations are almost certainly excessive.
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http://dx.doi.org/10.1111/j.1523-1739.2011.01662.xDOI Listing
June 2011

Effects of genetic captive-breeding protocols on sperm quality and fertility in the white-footed mouse.

Biol Reprod 2010 Oct 2;83(4):540-8. Epub 2010 Jun 2.

Center for Conservation and Evolutionary Genetics, National Zoological Park, Smithsonian Institution, Washington, DC, USA

Mice (Peromyscus leucopus noveboracensis) from a captive-breeding program were used to test the effects of three genetic breeding protocols (minimizing mean kinship [MK], random breeding, and selection for docility [DOC]) and inbreeding levels on sperm traits and fertility. Earlier, in generation 8, one DOC replicate went extinct because of poor reproductive success. By generation 10, spermatozoa from DOC mice had more acrosome and midpiece abnormalities, which were shown to be strong determinants of fertility, as well as lower sperm production and resistance to osmotic stress. In addition, determinants of fertility, including male and female components, were assessed in a comprehensive manner. Results showed that the probability (P) of siring litters is determined by sperm number, sperm viability, and midpiece and acrosome abnormalities; that the P of siring one versus two litters is determined by tail abnormalities; and that the total number of offspring is influenced by female size and proportion of normal sperm, showing the relative importance of different sperm traits on fertility. On average, males with 20% normal sperm sired one pup per litter, and males with 70% normal sperm sired eight pups per litter. Interestingly, the proportion of normal sperm was affected by docility but not by relatively low inbreeding. However, inbreeding depression in sperm motility was detected. In the MK group, inbreeding depression not only affected sperm motility but also fertility: An increase in the coefficient of inbreeding (f) of 0.03 reduced sperm motility by 30% and translated into an offspring reduction of three pups in second litters. A genetic load of 48 fecundity equivalents was calculated.
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http://dx.doi.org/10.1095/biolreprod.110.085316DOI Listing
October 2010

Methods and prospects for using molecular data in captive breeding programs: an empirical example using parma wallabies (Macropus parma).

J Hered 2009 Jul-Aug;100(4):441-54. Epub 2009 May 7.

Department of Conservation Science, Chicago Zoological Society, Brookfield, IL 60513, USA.

Zoo and aquarium breeding programs rely on accurate pedigrees to manage the genetics and demographics of captive populations. Breeding recommendations are often encumbered, however, by unknown parentage. If an individual has any amount of unknown ancestry, the relationships between that individual and all other individuals in a population are ambiguous, and breeding recommendations cannot be tailored to maximize genetic diversity and minimize inbreeding. In those situations, breeding program management might be improved by the incorporation of molecular data. We developed microsatellite markers for the parma wallaby (Macropus parma) and investigated how genetic data might be used to improve the management of the captive population. The parma wallaby is a small marsupial found in fragmented forests near the coast of New South Wales, Australia. Because the species is of conservation concern, the captive population in North America is managed by recurring breeding recommendations. The effectiveness of the population's management is hampered, however, because over half of the individuals have some amount of unknown ancestry. We used microsatellite data to resolve unknown parentage, described how molecular estimates of relatedness might inform future breeding recommendations, and used computer simulations to investigate how molecular estimates of relatedness among founders might contribute to the genetic management of the population. Our results indicated that microsatellite appraisals of parentage were useful with respect to clarifying pedigrees but that molecular assessments of founder relatedness provided very marginal benefits with regard to the preservation of genetic diversity and the avoidance of inbreeding.
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http://dx.doi.org/10.1093/jhered/esp019DOI Listing
September 2009

Rapid morphological and genetic change in Chicago-area Peromyscus.

Mol Ecol 2008 Jan 24;17(1):450-63. Epub 2007 Sep 24.

Department of Biological Sciences, University of Illinois at Chicago, 845 W. Taylor St., Chicago, IL 60607 USA.

We report rapid change of morphology and mitochondrial genes in white-footed mice (Peromyscus leucopus) in the Chicago (Illinois, USA) region. We sequenced mitochondrial DNA COX2 from 55 museum skins of white-footed mice caught in the Chicago area since 1855 and from 44 mice recently trapped in the same locations. We found consistent directional genotype replacement at five separate collection locations. We later focused on a single one of these locations (Volo Bog State Natural Area) and sequenced mitochondrial D-loop control region from 58 museum skins of mice collected in 1903-1976 and 32 mice recently trapped there. We found complete and more recent replacement of D-loop haplotypes, apparently occurring between 1976 and 2001. We tested whether these genetic changes were mirrored by changes in morphology by comparing 15 external and cranial traits. We found no significant morphological differences between mice collected in 1903-1976; however, mice collected in 2001-2003 showed 9 of 15 measurements to be significantly changed relative to the earlier samples. Recent mice were longer in total length, with broader, longer noses, and longer but shallower skulls(1). Discriminant function analysis allowed for 100% correct classification using these traits. Principal components analysis shows variance over time is well distributed across both external and cranial measures. The sequential replacements of haplotypes and the rapid change of morphology can best be explained by replacement of the regional population with immigrants from genetically distinct neighbouring populations, likely facilitated by the large environmental changes occurring over the time period. Replacement with genotypes from external populations may be a common mechanism of evolution of newly adaptive local forms in an increasingly human-impacted world.
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http://dx.doi.org/10.1111/j.1365-294X.2007.03517.xDOI Listing
January 2008