scholarly journals Reviewing the consequences of genetic purging on the success of rescue programs

2021 ◽  
Author(s):  
Noelia Pérez-Pereira ◽  
Armando Caballero ◽  
Aurora García-Dorado
Keyword(s):  
Inbreeding Depression ◽  
Extinction Risk ◽  
Conservation Strategy ◽  
Recessive Mutation ◽  
Stable Gene ◽  
Main Concern ◽  
Genetic Rescue ◽  
Genetic Purging ◽  
The Impact

AbstractGenetic rescue is increasingly considered a promising and underused conservation strategy to reduce inbreeding depression and restore genetic diversity in endangered populations, but the empirical evidence supporting its application is limited to a few generations. Here we discuss on the light of theory the role of inbreeding depression arising from partially recessive deleterious mutations and of genetic purging as main determinants of the medium to long-term success of rescue programs. This role depends on two main predictions: (1) The inbreeding load hidden in populations with a long stable demography increases with the effective population size; and (2) After a population shrinks, purging tends to remove its (partially) recessive deleterious alleles, a process that is slower but more efficient for large populations than for small ones. We also carry out computer simulations to investigate the impact of genetic purging on the medium to long term success of genetic rescue programs. For some scenarios, it is found that hybrid vigor followed by purging will lead to sustained successful rescue. However, there may be specific situations where the recipient population is so small that it cannot purge the inbreeding load introduced by migrants, which would lead to increased fitness inbreeding depression and extinction risk in the medium to long term. In such cases, the risk is expected to be higher if migrants came from a large non-purged population with high inbreeding load, particularly after the accumulation of the stochastic effects ascribed to repeated occasional migration events. Therefore, under the specific deleterious recessive mutation model considered, we conclude that additional caution should be taken in rescue programs. Unless the endangered population harbors some distinctive genetic singularity whose conservation is a main concern, restoration by continuous stable gene flow should be considered, whenever feasible, as it reduces the extinction risk compared to repeated occasional migration and can also allow recolonization events.

scholarly journals Reviewing the consequences of genetic purging on the success of rescue programs

2021 ◽  
Author(s):  
Noelia Perez-Pereira ◽  
Armando Caballero ◽  
Aurora Garcia-Dorado
Keyword(s):  
Inbreeding Depression ◽  
Extinction Risk ◽  
Conservation Strategy ◽  
Recessive Mutation ◽  
Stable Gene ◽  
Main Concern ◽  
Genetic Rescue ◽  
Genetic Purging ◽  
The Impact

Genetic rescue is increasingly considered a promising and underused conservation strategy to reduce inbreeding depression and restore genetic diversity in endangered populations, but the empirical evidence supporting its application is limited to a few generations. Here we discuss on the light of theory the role of inbreeding depression arising from partially recessive deleterious mutations and of genetic purging as main determinants of the medium to long-term success of rescue programs. This role depends on two main predictions: (1) The inbreeding load hidden in populations with a long stable demography increases with the effective population size; and (2) After a population shrinks, purging tends to remove its (partially) recessive deleterious alleles, a process that is slower but more efficient for large populations than for small ones. We also carry out computer simulations to investigate the impact of genetic purging on the medium to long term success of genetic rescue programs. For some scenarios, it is found that hybrid vigor followed by purging will lead to sustained successful rescue. However, there may be specific situations where the recipient population is so small that it cannot purge the inbreeding load introduced by migrants, which would lead to increased fitness inbreeding depression and extinction risk in the medium to long term. In such cases, the risk is expected to be higher if migrants came from a large non-purged population with high inbreeding load, particularly after the accumulation of the stochastic effects ascribed to repeated occasional migration events. Therefore, under the specific deleterious recessive mutation model considered, we conclude that additional caution should be taken in rescue programs. Unless the endangered population harbors some distinctive genetic singularity whose conservation is a main concern, restoration by continuous stable gene flow should be considered, whenever feasible, as it reduces the extinction risk compared to repeated occasional migration and can also allow recolonization events.

Inbreeding and Inbreeding Depression

2020 ◽  
Author(s):  
Donald M. Waller ◽  
Lukas F. Keller
Keyword(s):  
Genetic Variation ◽  
Inbreeding Depression ◽  
Charles Darwin ◽  
Extinction Risk ◽  
Random Mating ◽  
Genetic Material ◽  
Great Length ◽  
Genetic Rescue ◽  
Isolated Populations ◽  
Genetic Transmission

Inbreeding (also referred to as “consanguinity”) occurs when mates are related to each other due to incest, assortative mating, small population size, or population sub-structuring. Inbreeding results in an excess of homozygotes and hence a deficiency of heterozygotes. This, in turn, exposes recessive genetic variation otherwise hidden by heterozygosity with dominant alleles relative to random mating. Interest in inbreeding arose from its use in animal and plant breeding programs to expose such variation and to fix variants in genetically homogenous lines. Starting with Gregor Mendel’s experiments with peas, geneticists have widely exploited inbreeding as a research tool, leading R. C. Lewontin to conclude that “Every discovery in classical and population genetics has depended on some sort of inbreeding experiment” (see Lewontin’s 1965 article “The Theory of Inbreeding.” Science 150:1800–1801). Charles Darwin wrote an entire book on the effects of inbreeding as measured in fifty-two taxa of plants. He and others noted that most plants and animals go to great length to avoid inbreeding, suggesting that inbreeding has high costs that often outweigh the benefits of inbreeding. Benefits of inbreeding include increased genetic transmission while the costs of inbreeding manifest as inbreeding depression when deleterious, mostly recessive alleles otherwise hidden as heterozygotes emerge in homozygote form upon inbreeding. Inbreeding also reduces fitness when heterozygotes are more fit than both homozygotes, but such overdominance is rare. Recurrent mutation continuously generates deleterious recessive alleles that create a genetic “load” of deleterious mutations mostly hidden within heterozygotes in outcrossing populations. Upon inbreeding, the load is expressed when deleterious alleles segregate as homozygotes, causing often substantial inbreeding depression. Although inbreeding alone does not change allele frequencies, it does redistribute genetic variation, reducing it within families or populations while increasing it among families or populations. Inbreeding also increases selection by exposing deleterious recessive mutations, a process called purging that can deplete genetic variation. For all these reasons, inbreeding is a central concept in evolutionary biology. Inbreeding is also central to conservation biology as small and isolated populations become prone to inbreeding and thus suffer inbreeding depression. Inbreeding can reduce population viability and increase extinction risk by reducing individual survival and/or reproduction. Such effects can often be reversed, however, by introducing new genetic material that re-establishes heterozygosity (“genetic rescue”). The current availability of DNA sequence and expression data is now allowing more detailed analyses of the causes and evolutionary consequences of inbreeding.

scholarly journals Detecting inbreeding depression in a severely bottlenecked, recovering species: The little spotted kiwi (Apteryx owenii)

2021 ◽  
Author(s):  
◽  
Helen R. Taylor
Keyword(s):  
Genetic Variation ◽  
Population Growth ◽  
Inbreeding Depression ◽  
Hatching Success ◽  
Extinction Risk ◽  
Long Island ◽  
Island Population ◽  
Valuable Insight ◽  
Inbreeding Coefficients

<p>Population bottlenecks reduce genetic variation and population size. Small populations are at greater risk of inbreeding, which further erodes genetic diversity and can lead to inbreeding depression. Inbreeding depression is known to increase extinction risk. Thus, detecting inbreeding depression is important for population viability assessment and conservation management. However, identifying inbreeding depression in wild populations is challenging due to the difficulty of obtaining long-term measures of fitness and error-free measures of individual inbreeding coefficients. I investigated inbreeding depression and our power to detect it in species that have very low genetic variation, using little spotted kiwi (Apteryx owenii) (LSK) as a case study. This endemic New Zealand ratite experienced a bottleneck of, at most, five individuals ~100 years ago and has since been subjected to secondary bottlenecks as a result of introductions to new predator-free locations. There is no behavioural pedigree data available for any LSK population and the status of the species is monitored almost exclusively via population growth. I conducted two seasons of field work to determine hatching success in the two LSK populations with the highest and lowest numbers of founders; Zealandia Sanctuary (40 founders) and Long Island (two founders). I also used simulation-based modelling to assess the feasibility of reconstructing pedigrees based on individual genotypes from LSK populations to calculate pedigree inbreeding coefficients. Finally, I used microsatellite genotypes to measure the genetic erosion in successive filial groupings of Long Island and Zealandia LSK as a result of their respective bottlenecks, and tested for inbreeding depression on Long Island. Hatching success was significantly lower on Long Island than in Zealandia in both years of the study despite significantly higher reproductive effort on Long Island. Although this was suggestive of inbreeding depression on Long Island, simulation results showed that constructing a pedigree for any LSK population based on the genetic markers and samples currently available would lead to inaccurate pedigrees and invalid estimates of individual inbreeding coefficients. Thus, an alternative method of detecting inbreeding and inbreeding depression was required. Microsatellite data showed continued loss of heterozygosity in both populations, but loss of allelic diversity on Long Island only. Individual genotypes indicated that the majority (74%) of the adult Long Island population is comprised of the founding pair (F) and their direct offspring (F1) rather than birds from subsequent generations (F2+). This is not what would be expected if survival was equal between these two filial classes. I suggest that the high levels of inbreeding (≥0.25) in F2+ birds is impacting on their survival, creating a demographic skew in the population and resulting in lower hatching success on average on Long Island when compared to the relatively outbred Zealandia birds. This inbreeding depression appears to have been masked, thus far, by positive population growth on Long Island resulting from the long life span of LSK (27-83 years) and continued reproductive success of the founding pair. Thus, it is likely that the Long Island population will go into decline when the founding pair cease to reproduce. This study highlights the challenges of measuring inbreeding depression in species with very low genetic variation and the importance of assessing the statistical power and reliability of the genetic tools available for those species. It also demonstrates that basic genetic techniques can offer valuable insight when more advanced tools prove error-prone. Monitoring vital rates such as hatching success in conjunction with genetic data is important for assessing the success of conservation translocations and detecting potentially cryptic genetic threats such as inbreeding depression. My results suggest that LSK are being affected by inbreeding depression and that careful genetic management will be required to ensure the long-term viability of this species.</p>

scholarly journals A management plan for a declining population of the Souss valley tortoise in an arid steppe-land of west-central Morocco

2021 ◽  
Author(s):  
Hichami Nawal ◽  
MOHAMMED ZNARI
Keyword(s):  
Sex Ratio ◽  
Population Size ◽  
Extinction Risk ◽  
Management Plan ◽  
Habitat Destruction ◽  
North West ◽  
West Central ◽  
Arid Steppe ◽  
The Impact

The endangered Moorish tortoise Testudo graeca is the unique terrestrial chelonian species in North-west Africa. In west-central Morocco, the endemic subspecies, the Souss valley tortoise T. g. soussensis, occupies semi-arid to arid low-quality habitats, and is subject to serious threats. A long-term mark-recapture programme from 2001 to 2012 allowed estimating population size and structure, sex ratio, and survivorship in one of the well-known populations in a degraded and overgrazed arid steppe-land of west-central Morocco. Spring population size considerably decreased to more than half in less than 10 years, with a mean density lower than 3 ind.ha-1 in 2012 compared to its last known density estimat-ed in 2003. In spring 2012, the population structure exhibited an unbalanced male-biased sex ratio (61:39) and a scarcity of juveniles (<5%). We identified five major conservation problems in the study area: (i) habitat destruction and overgrazing; (ii) over-collecting of tortoises for pet trade , iii) direct dis-turbance; iv) tortoise handling mostly for field research, and v) increased extinction risk due to the small population size. We carried out a population viability analysis using the VORTEX software based on published and obtained data on population and life history parameters. With no management action, the population will go extinct during the forthcoming 40 years after the last estimate. The most efficient management option for a long-term persistence of the population would be reducing the nest and neo-nate mortality by 90%. To attenuate the impact of the threatening factors, we developed a management plan that includes population reinforcement and habitat restoration options. 

scholarly journals Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression

2019 ◽  
Author(s):  
Christopher C. Kyriazis ◽  
Robert K. Wayne ◽  
Kirk E. Lohmueller
Keyword(s):  
Genetic Diversity ◽  
Inbreeding Depression ◽  
Extinction Risk ◽  
Fragmented Landscape ◽  
Small Populations ◽  
Deleterious Mutations ◽  
Genetic Rescue ◽  
Isolated Populations ◽  
Large Populations ◽  
Source Populations

AbstractHuman-driven habitat fragmentation and loss have led to a proliferation of small and isolated plant and animal populations with high risk of extinction. One of the main threats to extinction in these populations is inbreeding depression, which is primarily caused by the exposure of recessive deleterious mutations as homozygous by inbreeding. The typical approach for managing these populations is to maintain high genetic diversity, often by translocating individuals from large populations to initiate a ‘genetic rescue.’ However, the limitations of this approach have recently been highlighted by the demise of the gray wolf population on Isle Royale, which was driven to the brink of extinction soon after the arrival of a migrant from the large mainland wolf population. Here, we use a novel population genetic simulation framework to investigate the role of genetic diversity, deleterious variation, and demographic history in mediating extinction risk due to inbreeding depression in small populations. We show that, under realistic models of dominance, large populations harbor high levels of recessive strongly deleterious variation due to these mutations being hidden from selection in the heterozygous state. As a result, when large populations contract, they experience a substantially elevated risk of extinction after these strongly deleterious mutations are exposed by inbreeding. Moreover, we demonstrate that although translocating individuals to small populations is broadly effective as a means to reduce extinction risk, using small or moderate-sized source populations rather than large source populations can greatly increase the effectiveness of genetic rescue due to greater purging in these smaller populations. Our findings challenge the traditional conservation paradigm that focuses on maximizing genetic diversity to reduce extinction risk in favor of a view that emphasizes minimizing strongly deleterious variation. These insights have important implications for managing small and isolated populations in the increasingly fragmented landscape of the Anthropocene.Impact SummaryNumerous threats to extinction exist for small populations, including the detrimental effects of inbreeding. Although much of the focus in reducing these harmful effects in small populations has been on maintaining high genetic diversity, here we use simulations to demonstrate that emphasis should instead be placed on minimizing strongly deleterious variation. More specifically, we show that historically-large populations with high levels of genetic diversity also harbor elevated levels of recessive strongly deleterious mutations hidden in the heterozygous state. Thus, when these populations contract, inbreeding can expose these strongly deleterious mutations as homozygous and lead to severe inbreeding depression and rapid extinction. Moreover, we demonstrate that, although translocating individuals to these small populations to perform a ‘genetic rescue’ is broadly beneficial, the effectiveness of this strategy can be greatly increased by targeting historically-smaller source populations where recessive strongly deleterious mutations have been purged. These results challenge long-standing views on how to best conserve small and isolated populations facing the threat of inbreeding depression, and have immediate implications for preserving biodiversity in the increasingly fragmented landscape of the Anthropocene.

scholarly journals Genomic signatures of inbreeding and genetic load in a threatened rattlesnake

2021 ◽  
Author(s):  
Alexander Ochoa ◽  
H. Lisle Gibbs
Keyword(s):  
Threatened Species ◽  
Empirical Studies ◽  
Genetic Load ◽  
Population History ◽  
Deleterious Mutations ◽  
Genetic Rescue ◽  
Isolated Populations ◽  
Genome Wide ◽  
The Impact

Theory predicts that threatened species living in small populations will experience high levels of inbreeding that will increase their negative genetic load but recent work suggests that the impact of load may be minimized by purging resulting from long term population bottlenecks. Empirical studies that examine this idea using genome-wide estimates of inbreeding and genetic load in threatened species are limited. Here we use genome resequencing data to compare levels of inbreeding, levels of genetic load and population history in threatened Eastern massasauga rattlesnakes (Sistrurus catenatus) which exist in small isolated populations and closely-related yet outbred Western massasauga rattlesnakes (S. tergeminus). In terms of inbreeding, S. catenatus genomes had a greater number of ROHs of varying sizes indicating sustained inbreeding through repeated bottlenecks when compared to S. tergeminus. At the species level, outbred S. tergeminus had higher genome-wide levels of genetic load in the form of greater numbers of derived deleterious mutations compared to S. catenatus presumably due to long-term purging of deleterious mutations in S. catenatus. In contrast, mutations that escaped the “drift sieve” and were polymorphic within S. catenatus populations were more abundant and more often found in homozygote genotypes than in S. tergeminus suggesting a reduced efficiency of purifying selection in smaller S. catenatus populations. Our results support an emerging idea that the historical demography of a threatened species has a significant impact on the type of genetic load present which impacts implementation of conservation actions such as genetic rescue.

scholarly journals Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation

2020 ◽  
pp. 201909599
Author(s):  
Alina K. Niskanen ◽  
Anna M. Billing ◽  
Håkon Holand ◽  
Ingerid J. Hagen ◽  
Yimen G. Araya-Ajoy ◽  
...  
Keyword(s):  
Inbreeding Depression ◽  
House Sparrow ◽  
Extinction Risk ◽  
Demographic History ◽  
Natural Populations ◽  
Ecological Factors ◽  
Genomic Tools ◽  
Subdivided Populations ◽  
Modern Genomic

Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations.

Reduced recruitment performance in natural populations of anadromous salmonids associated with hatchery-reared fish

2011 ◽  
Vol 68 (3) ◽  
pp. 511-522 ◽  
Author(s):  
M. W. Chilcote ◽  
K. W. Goodson ◽  
M. R. Falcy
Keyword(s):  
Reproductive Performance ◽  
Coho Salmon ◽  
Natural Populations ◽  
Negative Relationship ◽  
Conservation Strategy ◽  
Steelhead Trout ◽  
Hatchery Fish ◽  
The Impact ◽  
Recruitment Performance

We found a negative relationship between the reproductive performance in natural, anadromous populations of steelhead trout ( Oncorhynchus mykiss ), coho salmon ( O. kisutch ), and Chinook salmon ( O. tshawytscha ), and the proportion of hatchery fish in the spawning population. We used intrinsic productivity as estimated from fitting a variety of recruitment models to abundance data for each population as our indicator of reproductive performance. The magnitude of this negative relationship is such that we predict the recruitment performance for a population composed entirely of hatchery fish would be 0.128 of that for a population composed entirely of wild fish. The effect of hatchery fish on reproductive performance was the same among all three species. Further, the impact of hatchery fish from “wild type” hatchery broodstocks was no less adverse than hatchery fish from traditional, domesticated broodstocks. We also found no support for the hypothesis that a population's reproductive performance was affected by the length of exposure to hatchery fish. In most cases, measures that minimize the interactions between wild and hatchery fish will be the best long-term conservation strategy for wild populations.

scholarly journals Detecting inbreeding depression in a severely bottlenecked, recovering species: The little spotted kiwi (Apteryx owenii)

2021 ◽  
Author(s):  
◽  
Helen R. Taylor
Keyword(s):  
Genetic Variation ◽  
Population Growth ◽  
Inbreeding Depression ◽  
Hatching Success ◽  
Extinction Risk ◽  
Long Island ◽  
Island Population ◽  
Valuable Insight ◽  
Inbreeding Coefficients

<p>Population bottlenecks reduce genetic variation and population size. Small populations are at greater risk of inbreeding, which further erodes genetic diversity and can lead to inbreeding depression. Inbreeding depression is known to increase extinction risk. Thus, detecting inbreeding depression is important for population viability assessment and conservation management. However, identifying inbreeding depression in wild populations is challenging due to the difficulty of obtaining long-term measures of fitness and error-free measures of individual inbreeding coefficients. I investigated inbreeding depression and our power to detect it in species that have very low genetic variation, using little spotted kiwi (Apteryx owenii) (LSK) as a case study. This endemic New Zealand ratite experienced a bottleneck of, at most, five individuals ~100 years ago and has since been subjected to secondary bottlenecks as a result of introductions to new predator-free locations. There is no behavioural pedigree data available for any LSK population and the status of the species is monitored almost exclusively via population growth. I conducted two seasons of field work to determine hatching success in the two LSK populations with the highest and lowest numbers of founders; Zealandia Sanctuary (40 founders) and Long Island (two founders). I also used simulation-based modelling to assess the feasibility of reconstructing pedigrees based on individual genotypes from LSK populations to calculate pedigree inbreeding coefficients. Finally, I used microsatellite genotypes to measure the genetic erosion in successive filial groupings of Long Island and Zealandia LSK as a result of their respective bottlenecks, and tested for inbreeding depression on Long Island. Hatching success was significantly lower on Long Island than in Zealandia in both years of the study despite significantly higher reproductive effort on Long Island. Although this was suggestive of inbreeding depression on Long Island, simulation results showed that constructing a pedigree for any LSK population based on the genetic markers and samples currently available would lead to inaccurate pedigrees and invalid estimates of individual inbreeding coefficients. Thus, an alternative method of detecting inbreeding and inbreeding depression was required. Microsatellite data showed continued loss of heterozygosity in both populations, but loss of allelic diversity on Long Island only. Individual genotypes indicated that the majority (74%) of the adult Long Island population is comprised of the founding pair (F) and their direct offspring (F1) rather than birds from subsequent generations (F2+). This is not what would be expected if survival was equal between these two filial classes. I suggest that the high levels of inbreeding (≥0.25) in F2+ birds is impacting on their survival, creating a demographic skew in the population and resulting in lower hatching success on average on Long Island when compared to the relatively outbred Zealandia birds. This inbreeding depression appears to have been masked, thus far, by positive population growth on Long Island resulting from the long life span of LSK (27-83 years) and continued reproductive success of the founding pair. Thus, it is likely that the Long Island population will go into decline when the founding pair cease to reproduce. This study highlights the challenges of measuring inbreeding depression in species with very low genetic variation and the importance of assessing the statistical power and reliability of the genetic tools available for those species. It also demonstrates that basic genetic techniques can offer valuable insight when more advanced tools prove error-prone. Monitoring vital rates such as hatching success in conjunction with genetic data is important for assessing the success of conservation translocations and detecting potentially cryptic genetic threats such as inbreeding depression. My results suggest that LSK are being affected by inbreeding depression and that careful genetic management will be required to ensure the long-term viability of this species.</p>

scholarly journals Genetic purging in captive endangered ungulates with extremely low effective population sizes

Heredity ◽  
2021 ◽  
Author(s):  
Eugenio López-Cortegano ◽  
Eulalia Moreno ◽  
Aurora García-Dorado
Keyword(s):  
Natural Selection ◽  
Population Size ◽  
Inbreeding Depression ◽  
Captive Breeding ◽  
Random Mating ◽  
Management Strategies ◽  
Effective Population ◽  
Population Sizes ◽  
Genetic Purging

AbstractInbreeding threatens the survival of small populations by producing inbreeding depression, but also exposes recessive deleterious effects in homozygosis allowing for genetic purging. Using inbreeding-purging theory, we analyze early survival in four pedigreed captive breeding programs of endangered ungulates where population growth was prioritized so that most adult females were allowed to contribute offspring according to their fitness. We find evidence that purging can substantially reduce inbreeding depression in Gazella cuvieri (with effective population size Ne = 14) and Nanger dama (Ne = 11). No purging is detected in Ammotragus lervia (Ne = 4), in agreement with the notion that drift overcomes purging under fast inbreeding, nor in G. dorcas (Ne = 39) where, due to the larger population size, purging is slower and detection is expected to require more generations. Thus, although smaller populations are always expected to show smaller fitness (as well as less adaptive potential) than larger ones due to higher homozygosis and deleterious fixation, our results show that a substantial fraction of their inbreeding load and inbreeding depression can be purged when breeding contributions are governed by natural selection. Since management strategies intended to maximize the ratio from the effective to the actual population size tend to reduce purging, the search for a compromise between these strategies and purging could be beneficial in the long term. This could be achieved either by allowing some level of random mating and some role of natural selection in determining breeding contributions, or by undertaking reintroductions into the wild at the earliest opportunity.

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