Founder Effects,Inbreeding, and Loss of Genetic Diversity in Four Avian Reintroduction Programs

Abstract: The number of individuals translocated and released as part of a reintroduction is often small, as is the final established population, because the reintroduction site is typically small. Small founder and small resulting populations can result in population bottlenecks, which are associated with increased rates of inbreeding and loss of genetic diversity, both of which can affect the long‐term viability of reintroduced populations. I used information derived from pedigrees of four monogamous bird species reintroduced onto two different islands (220 and 259 ha) in New Zealand to compare the pattern of inbreeding and loss of genetic diversity among the reintroduced populations. Although reintroduced populations founded with few individuals had higher levels of inbreeding, as predicted, other factors, including biased sex ratio and skewed breeding success, contributed to high levels of inbreeding and loss of genetic diversity. Of the 10–58 individuals released, 4–25 genetic founders contributed at least one living descendent and yielded approximately 3–11 founder–genome equivalents (number of genetic founders assuming an equal contribution of offspring and no random loss of alleles across generations) after seven breeding seasons. This range is much lower than the 20 founder–genome equivalents recommended for captive‐bred populations. Although the level of inbreeding in one reintroduced population initially reached three times that of a closely related species, the long‐term estimated rate of inbreeding of this one population was approximately one‐third that of the other species due to differences in carrying capacities of the respective reintroduction sites. The increasing number of reintroductions to suitable areas that are smaller than those I examined here suggests that it might be useful to develop long‐term strategies and guidelines for reintroduction programs, which would minimize inbreeding and maintain genetic diversity.     

Genetic Effects of Multiple Generations of Supportive Breeding

Abstract: The practice of supporting weak wild populations by capturing a fraction of the wild individuals, bringing them into captivity for reproduction, and releasing their offspring into the natural habitat to mix with wild ones is called supportive breeding and has been widely applied in the fields of conservation biology and fish and wildlife management. This procedure is intended to increase population size without introducing exogenous genes into the managed population. Previous work examining the genetic effects of a single generation of supportive breeding has shown that although a successful program increases the census population size, it may reduce the genetically effective population size and thereby induce excessive inbreeding and loss of genetic variation. We expand and generalize previous analyses of supportive breeding and consider the effects of multiple generations of supportive breeding on rates of inbreeding and genetic drift. We derived recurrence equations for the inbreeding coefficient and coancestry, and thereby equations for inbreeding and variance effective sizes, under three models for selecting captive breeders: at random, preferentially among those born in captivity, and preferentially among those born in the wild. Numerical examples indicate that supportive breeding, when carried out successfully over multiple generations, may increase not only the census but also the effective size of the supported population as a whole. If supportive breeding does not result in a substantial and continuous increase of the census size of the breeding population, however, it might be genetically harmful because of elevated rates of inbreeding and genetic drift.     

Estimation of kinship parameters: the island model with separate sexes

Summary Information from pedigrees provides the most accurate means of estimating relatedness within and between social groups, but the method has the disadvantage of requiring longterm breeding records. If a regular system of mating occurs, then kinship parameters may be estimated from recurrence relations which decribe the change in coancestry and inbreeding from generation to generation. Breeding records collected over a single generation are therefore sufficient. In this paper the island model is used for the derivation of general expression of the coancestry and inbreeding coefficients in a dioecious population with non-overlapping generations. An equation for the average coefficient of coancestry (f ^JJ ) within a juvenile cohort is first found, and the other coefficients are then easily obtained. Parameters required are the inbreeding effective numbers of male and female parents and the migration rates of the two sexes. — In species with overlapping generations, the average coefficient of coancestry of the juvenile cohort is not related simply by migration rates to the average coancestries of the adult classes. The difference arises because average coancestry between pairs of individuals chosen from different cohorts is not in general the same as that between pairs of the same cohort. The precise difference depends on the mating system and cohort structure of the social group. Suitable modification to the basic expression for f ^JJ is described. The use of the composite method is illustrated by reference to the social units of two large mammals: prides of lion and clans of impala.     

Population Viability Analysis for a Small Population of Red-Cockaded Woodpeckers and an Evaluation of Enhancement Strategies

We performed a series of population and pedigree analyses to examine the viability of a small Red-cockaded Woodpecker ( Picoides borealis ) population located at the Savannah River Site, in Barnwell and Aiken counties of South Carolina. The population's existence and future survival are precarious. As few as four individuals, including just one breeding pair, comprised this population in 1985. Now, primarily because of experimental transformation of birds from other areas, the population has increased to 25. As of 1990, genealogy pedigree analysis showed that the respective contribution of 14 founders to the extant population has not been equal. Founder gender equivalents are low (5.4) but could reach 9.2 if poorly-represented founders were to produce offspring. The fraction of founder gene diversity retained in the current population is 0.91. Successful recovery strategies would ensure 95% probability of population survival while maintaining 90% heterozygosity for 200 years. Viability analyses indicated that, depending on relative effects of inbreeding depression and stochastic environmental events, the Savannah River Site population has a 68–100% chance of extinction during this period. Annual translocation into the population of at least three females and two males for a 10-year period will achieve a 96% probability of survival for 200 years. Even with translocation of numerous males and females per year (up to 50 of each), the 90% heterozygosity goal may not be achieved. We discuss recommendations for choosing individuals for translocation logistical constraints on achieving recovery objectives, and limitations of our modeling approach.     

Supportive Breeding and Variance Effective Population Size

The practice of supporting weak, wild populations through release of individuals bred in captivity is becoming an increasingly important conservation measure. A frequently recommended form of such breeding-release activity refers to supportive breeding: a fraction of the target population is brought into captivity for reproduction, and the resulting progeny are released to mix with the wild segment of the population. We derived an expression for the variance effective size of a population managed through supportive breeding and discuss its relationship to previously published equations that are based on the assumption of random mating. We show that the effect of supportive breeding may be quite different on the inbreeding and the variance effective sizes. Whereas supportive breeding always results in a reduction of the inbreeding effective number, the variance effective number may either decrease, increase, or remain unchanged. We discuss these observations in relation to conservation management and suggest some general guidelines for supportive breeding situations. Our recommendations include making a distinction between inbreeding and variance effective numbers; taking particular care when dealing with organisms with high reproductive potential; assuring that the amount of drift be no larger than it would be without supportive breeding; and focusing primarily on the variance effective size of a population-that is, on the effective number directly related to the rate of loss of gene diversity.     

Relative Contribution of Inbreeding Depression and Eroded Adaptive Diversity to Extinction Risk in Small Populations of Shore Campion

Abstract:  To study the relative importance of inbreeding depression and the loss of adaptive diversity in determining the extinction risk of small populations, we carried out an experiment in which we crossed and self-fertilized founder plants from a single, large population of shore campion ( Silene littorea Brot.). We used the seeds these plants produced to colonize 18 new locations within the distribution area of the species. The reintroduced populations were of three kinds: inbred and genetically homogeneous, each made up of selfed seed from a single plant; inbred and mixed, made up of a mixture of selfed seeds from all founder plants; and outbred and mixed, made up of a mixture of seeds obtained in outcrosses between the founders. We compared the inbred homogeneous populations with the inbred mixed to measure the effect of genetic diversity among individuals and the inbred mixed with the outbred mixed to measure the effect of inbreeding. Reintroduction success was seriously limited by inbreeding, whereas it was not affected by genetic diversity. This observation and the nonsignificant interaction between family and reintroduction location for individual plant characters suggest that the fixation of overall deleterious genes causing inbreeding depression posed a more serious threat to the short-term survival of the populations than the loss of genes involved in genotype and environment interactions. Thus, reintroduction success was related to adaptive diversity. Preventing such fixation might be the most important consideration in the genetic management and conservation of shore campion populations.     

Effect of Migration or Inbreeding Followed by Selection on Low-Founder-Number Populations: Implications for Captive Breeding Programs

Using the housefly, Musca domestica (L), as a model system, we tested the ability of two extremes in the range of possible captive breeding protocols to yield sustainable populations following founding with low founder numbers. The protocols tested included two levels of migration as well as inbreeding followed by selection, each with appropriate controls. Each low-founder-number population was founded with two pairs of flies. The maximum migration scheme had 50% migration per generation, and the minimum migration populations experienced a migration rate of 2.5% per generation. The control level of migration was 0%. A fourth low-founder-number treatment was designed to test the effect of inbreeding followed by selection. Two sets of high-founder-number control groups were also derived from the stock population. Two fitness measures, viability and productivity of the populations, were recorded at the fifth generation. Populations in the minimum-migration and zero migration treatment groups had lower fitness than populations in any other treatment for both measures. Populations that experienced inbreeding and selection for high fitness levels, high levels of migration, or large high-founder-number populations were equally fit. These results demonstrate that a captive-breeding scheme that contains substantial levels of migration or inbreeding followed by selection can yield highly adapted populations.     

Modeling Problems in Conservation Genetics Using Captive Drosophila Populations: Consequences of Equalization of Family Sizes

Equalization of family sizes is recommended for use in captive breeding programs, as it is predicted to double effective population sizes, reduce inbreeding, and slow the loss of genetic variation. The effects of maintaining small captive populations with equalization of family sizes versus random choice of parents on levels of inbreeding genetic variation, reproductive fitness, and effective population sizes ( N _e) were evaluated in 10 lines of each treatment maintained with four pairs of parents per generation. The mean inbreeding coefficient ( F ) increased at a significantly slower rate with equalization than with random choice (means of 0.35 and 0.44 at generation 10). Average heterozygosities at generation 10, based on six polymorphic enzyme loci, were significantly higher with equalization (0.149) than with random choice (0.085), compared to the generation 0 level of 0.188. The competitive index measure of reproductive fitness at generation 11 was more than twice as high with equalization as with random choice, both being much lower than in the outbred base population. There was considerable variation among replicate lines within treatments in all the above measures and considerable overlap between lines from the two treatments. Estimates of N _e for equalization were greater than those for random choice, whether estimated from changes in average heterozygosities or from changes in F. Equalization of family sizes can be unequivocally recommended for use in the genetic management of captive populations.     

Genetic Analyses Through DNA Fingerprinting of Captive Populations of Hawaiian Geese

DNA fingerprinting was used to assess levels of genetic variation in 106 Hawaiian Geese, or Nene ( Branta sandvicensis ), from two captive colonies in Hawaii and Slimbridge, England. Mantel tests were used to determine differences in mean similarity coefficients obtained from DNA fingerprints between unrelated and related Nene within and between captive colonies and to determine whether pedigree-based estimates of relatedness correlated with DNA fingerprint-based estimates. Between colonies, mean similarity coefficients for unrelated and related Slimbridge Nene were higher than those for Hawaiian Nene. Within each colony, related Nene bad higher mean similarity coefficients than did unrelated Nene. A positive relationship was found between coancestry coefficients and similarity coefficients. A greater number of founders for the Hawaiian colony contributed to the lower mean similarity coefficients. As genetic variation decreases, difficulty in distinguishing relatedness among individuals using DNA fingerprinting may increase. Lower genetic variation also may increase tine error in estimating the relationship between coancestry and similarity coefficients. DNA fingerprinting of Nene identified unique alleles and can determine optimal pairings between individuals. The calibrated similarity coefficient distributions can help determine the relatedness of individuals in wild populations of Nene.     

Hereditary Blindness in a Captive Wolf (Canis lupus) Population: Frequency Reduction of a Deleterious Allele in Relation to Gene Conservation

Numerous cases of hereditary diseases and disorders have been reported in wild animals bred in captivity, but little attention has been paid to the particular genetic management problems that arise when such defects occur. These problems include the obstacle of eliminating the deleterious allele(s) without contemporary loss of genetic variability. In this paper we use the statistical methods of pedigree analysis to address questions regarding a previously presumed hereditary form of blindness observed in a captive wolf population bred for conservation purposes in Scandinavian zoos. The most likely mode of inheritance coincides with an autosomal recessive allele with either a full penetrance or a reduced penetrance of 0.6 (depending on the reliability of studbook records). Using these two models of inheritance, we calculate the probability of carrying the blindness allele for each living animal. Analysis of the effect of removing high-probability carriers on founder allele survival and level of inbreeding demonstrates that the frequency of the deleterious allele can be significantly reduced without seriously affecting founder allele survival or current degree of inbreeding in the wolf population.     

Inbreeding and Loss of Genetic Variation in a Reintroduced Population of Mauritius Kestrel

Abstract:  Many populations have recovered from severe bottlenecks either naturally or through intensive conservation management. In the past, however, few conservation programs have monitored the genetic health of recovering populations. We conducted a conservation genetic assessment of a small, reintroduced population of Mauritius Kestrel ( Falco punctatus ) to determine whether genetic deterioration has occurred since its reintroduction. We used pedigree analysis that partially accounted for individuals of unknown origin to document that (1) inbreeding occurred frequently (2.6% increase per generation; N _eI= 18.9), (2) 25% of breeding pairs were composed of either closely or moderately related individuals, (3) genetic diversity has been lost from the population (1.6% loss per generation; N _eV= 32.1) less rapidly than the corresponding increase in inbreeding, and (4) ignoring the contribution of unknown individuals to a pedigree will bias the metrics derived from that pedigree, ultimately obscuring the prevailing genetic dynamics. The rates of inbreeding and loss of genetic variation in the subpopulation of Mauritius Kestrel we examined were extreme and among the highest yet documented in a wild vertebrate population. Thus, genetic deterioration may affect this population's long-term viability. Remedial conservation strategies are needed to reduce the impact of inbreeding and loss of genetic variation in this species. We suggest that schemes to monitor genetic variation after reintroduction should be an integral component of endangered species recovery programs.     

Inbreeding Depression in the Speke's Gazelle Captive Breeding Program

Abstract: The Speke's gazelle ( Gazella spekei ) captive breeding program has been presented as one of the few examples of selection reducing the genetic load of a population and as a potential model for the captive breeding of endangered species founded from a small number of individuals. In this breeding program, three generations of mate selection apparently increased the viability of inbred individuals. We reanalyzed the Speke's gazelle studbook and examined potential causes for the reduction of inbreeding depression. Our analysis indicates that the decrease in inbreeding depression is not consistent with any model of genetic improvement in the herd. Instead, we found that the effect of inbreeding decreased from severe to moderate during the first generation of inbreeding, and that this change is responsible for almost all of the decline in inbreeding depression observed during the breeding program. This eliminates selection as a potential explanation for the decrease in inbreeding depression and suggests that inbreeding depression may be more sensitive to environmental influences than is usually thought.     

Experimental Evidence for Beneficial Fitness Effects of Gene Flow in Recently Isolated Populations

Abstract: A rich theory has been developed to explain the evolution of populations at equilibrium conditions of gene flow, inbreeding, and selection. There are, however, few empirical examples of the effects of gene flow into recently isolated, small populations under nonequilibrium conditions, such as are expected following population fragmentation. We studied the effects of inbreeding and gene flow in small, experimental populations of the mustard Brassica campestris ( rapa ). Replicate populations of five individuals randomly mated in a growth room received treatments of 0, 1, or 2.5 migrants each generation. Plants from the sixth experimental generation were planted in an outdoor common garden to evaluate the effects of the treatments on fitness and the distribution of phenotypic variation. Regression of six fitness components on inbreeding coefficients indicated a negative effect of inbreeding on fitness for five of these components. The 0-migrant treatment had significantly lower fitness than the migrant treatments for four of six fitness components, but fitness did not differ between the 1-migrant and 2.5-migrant treatments. Phenotypic divergence among populations decreased with an increased number of migrants. These data provide empirical evidence of the beneficial fitness effects of a small number of migrants for recently fragmented populations.     

Family dynasties in the Tasmanian native hen (Gallinula mortierii)

For species that form multi-generational and territorial family groups, resource-rich areas are predicted to support family dynasties in which one genetic lineage continuously occupies an area and may even expand to occupy surrounding areas. Data from a long-term study of Tasmanian native hens (Gallinula mortierii) support this prediction. The reproductive success and dispersal patterns of 18 hen lineages were monitored for seven breeding seasons and over several generations. The founder group with the highest average territory quality produced the highest total number of fledged young and the highest number of fledged linear descendants, accounting for 24% of the combined reproductive output of these 18 lineages. In the space of 6 years, this single genetic lineage expanded from one territory to occupy 12 of the 47 territories present in the population. This rate of expansion was over four times the population average for the same period. A multivariate analysis revealed that the success of a genetic lineage depended only on the number of high-quality territories surrounding the founder group. These results further demonstrate the resource-dependent nature of reproductive success in this species, and also highlight the potential importance of family dynasties in other cooperative species with complex social dynamics and dispersal patterns.     

Inbreeding in a lek-mating ant species, Pogonomyrmex occidentalis

In this paper we have two goals. First, we examine the effects of sample size on the statistical power to detect a given amount of inbreeding in social insect populations. The statistical power to detect a given level of inbreeding is largely a function of the number of colonies sampled. We explore two sampling schemes, one in which a single individual per colony is sampled for different sample sizes and a second sampling scheme in which constant sampling effort is maintained (the product of the number of colonies and the number of workers per colony is constant). We find that adding additional workers to a sample from a colony makes it easier to detect inbreeding in samples from given number of colonies; however, adding more colonies rather than more workers per colony always gives greater power to detect inbreeding. Because even relatively large amounts of sib-mating generate relatively small inbreeding coefficients, detection of even substantial deviations from random mating will require very large samples. Second, we look at the amount of inbreeding in a large population of the western harvest ant, Pogonomyrmex occidentalis. We find deviations from Hardy-Weinberg equilibrium equivalent to approximately 27% sib-mating in our population ( f = 0.09). Review of past studies on the population structure of other Pogonomyrmex species suggests that inbreeding may be a regular feature of the mating system of these ants. Although P. occidentalisis a swarm-mating species, there are a number of features of its population biology which suggest that the effective population size may be small. These include topographical variation that potentially breaks the population into demes, variation in the reproductive output of colonies, and variation in the size of reproductives produced by colonies. Received: 6 May 1996 / Accepted after revision: 6 October 1996     

Heterozygosity‐Fitness Correlations and Inbreeding Depression in Two Critically Endangered Mammals

The relation among inbreeding, heterozygosity, and fitness has been studied primarily among outbred populations, and little is known about these phenomena in endangered populations. Most researchers conclude that the relation between coefficient of inbreeding estimated from pedigrees and fitness traits (inbreeding‐fitness correlations) better reflects inbreeding depression than the relation between marker heterozygosity and fitness traits (heterozygosity‐fitness correlations). However, it has been suggested recently that heterozygosity‐fitness correlations should only be expected when inbreeding generates extensive identity disequilibrium (correlations in heterozygosity and homozygosity across loci throughout the genome). We tested this hypothesis in Mohor gazelle (Gazella dama mhorr) and Iberian lynx (Lynx pardinus). For Mohor gazelle, we calculated the inbreeding coefficient and measured heterozygosity at 17 microsatellite loci. For Iberian lynx, we measured heterozygosity at 36 microsatellite loci. In both species we estimated semen quality, a phenotypic trait directly related to fitness that is controlled by many loci and is affected by inbreeding depression. Both species showed evidence of extensive identity disequilibrium, and in both species heterozygosity was associated with semen quality. In the Iberian lynx the low proportion of normal sperm associated with low levels of heterozygosity was so extreme that it is likely to limit the fertility of males. In Mohor gazelle, although heterozygosity was associated with semen quality, inbreeding coefficient was not. This result suggests that when coefficient of inbreeding is calculated on the basis of a genealogy that begins after a long history of inbreeding, the coefficient of inbreeding fails to capture previous demographic information because it is a poor estimator of accumulated individual inbreeding. We conclude that among highly endangered species with extensive identity disequilibrium, examination of heterozygosity‐fitness correlations may be an effective way to detect inbreeding depression, whereas inbreeding‐fitness correlations may be poor indicators of inbreeding depression if the pedigree does not accurately reflect the history of inbreeding. Correlaciones Heterocigosidad‐ Adaptabilidad y Depresión Endogámica en Dos Especies de Mamíferos Críticamente en Peligro     

Experimental Tests of Captive Breeding for Endangered Species

Abstract: Several captive breeding regimes were compared for their ability to maintain fitness ( larval viability) and genetic variation in small populations of the housefly ( Musca domestica L.). Populations were either maintained at constant sizes of 40, 200, or 2000 individuals or initiated with two pairs of flies and allowed to grow to 40 individuals ( low-founder-number populations). Low-founder-number populations without migration exhibited low larval viability (22%) after 24 generations, compared to larger populations maintained at either 200 (49%) or 2000 (69%) individuals, and suffered high extinction, with only 44% of the lines surviving 24 generations. Low-founder-number populations subjected to two additional founder ( bottleneck) episodes, reducing them to two pairs of flies, suffered little additional loss in fitness or extinction compared to the single-founder treatments. Migration as low as one individual per generation (2.5% migration) significantly offset both reduced fitness and rate of extinction. Conversely, fitness was not significantly increased for low-founder-number populations when founders were selected from the top performing 20% of pairs under full-sib mating. Populations maintained at 40 individuals were not sustainable, exhibiting low larval viability (35%) and a high extinction rate (40%) over 24 generations, similar to the extinction rates for populations initiated with only four founders. Although none of the populations maintained at 200 individuals went extinct, their fitness was reduced by 20% compared to a large control population maintained at 2000 individuals. Electrophoretic variation was significantly correlated with fitness across treatments, but the correlation of fitness to narrow-sense heritability of two morphometric traits was not significant.     

Breed Structures of for Conservation of Middle Rare Pigs: Implications the Berkshire, Tamworth, White, Large Black, Gloucester Old Spot, British Saddleback, and British Lop

Abstract: Registration details of seven rare British breeds of pig w e studied over the period 1978–1986 inclusive. For four breeds, numbers of pigs registered have shown a slight upward trend. About 70% of males and 40% of females that breed, do so in herds other than the natal herd In the breed for which most pedigree data were analysed (the British Lop), 95–100% of recent pig crops were inbred In the rare breeds generally, mean inbreeding at around 6% signifies an inbreeding rate of about 1 % per generation, higher than has been found in commercial breeds. Breeds did not differ greatly in the ways they were structured.
About a third of herds supplied boars to other herds, a relatively high proportion, indicating that the breeds have a structure that is not completely hierarchical, and this is favorable for genetic conservation. Pigs whose parents were from different herds were significantly less inbred than those with both parents from the same herd In some breeds it was clear that pigs sharing the same bloodline name were more closely related than pigs within the same herd but with different bloodline names.
Conservation procedures applied to these pigs have been designed to conform with the customs and procedures of the British pedigree livestock industry. The most important single such procedure is the registration, with a central authority, of breeding stock.     

Cover Caption

Cover : The Takahe (Porphyrio hochstetteri), once widespread throughout New Zealand, was thought to be extinct by the end of the 1800s. In 1948 a remnant population was rediscovered in a remote region of the country's South Island. As of 2007, 72 birds descended from 18 founders were distributed across 4 islands off the coast of New Zealand. Grueber et al. (pages 1617‐1625) evaluated the effect of inbreeding depression across all life‐history stages of the Takahe. Although levels at each stage were low, accumulated inbreeding depression ultimately reduced long‐term fitness. These results suggest that even species with high historical levels of inbreeding can lose fitness as a result of recent inbreeding.     

Translating effects of inbreeding depression on component vital rates to overall population growth in endangered bighorn sheep

Evidence of inbreeding depression is commonly detected from the fitness traits of animals, yet its effects on population growth rates of endangered species are rarely assessed. We examined whether inbreeding depression was affecting Sierra Nevada bighorn sheep (Ovis canadensis sierrae), a subspecies listed as endangered under the U.S. Endangered Species Act. Our objectives were to characterize genetic variation in this subspecies; test whether inbreeding depression affects bighorn sheep vital rates (adult survival and female fecundity); evaluate whether inbreeding depression may limit subspecies recovery; and examine the potential for genetic management to increase population growth rates. Genetic variation in 4 populations of Sierra Nevada bighorn sheep was among the lowest reported for any wild bighorn sheep population, and our results suggest that inbreeding depression has reduced adult female fecundity. Despite this population sizes and growth rates predicted from matrix-based projection models demonstrated that inbreeding depression would not substantially inhibit the recovery of Sierra Nevada bighorn sheep populations in the next approximately 8 bighorn sheep generations (48 years). Furthermore, simulations of genetic rescue within the subspecies did not suggest that such activities would appreciably increase population sizes or growth rates during the period we modeled (10 bighorn sheep generations, 60 years). Only simulations that augmented the Mono Basin population with genetic variation from other subspecies, which is not currently a management option, predicted significant increases in population size. Although we recommend that recovery activities should minimize future losses of genetic variation, genetic effects within these endangered populations-either negative (inbreeding depression) or positive (within subspecies genetic rescue)-appear unlikely to dramatically compromise or stimulate short-term conservation efforts. The distinction between detecting the effects of inbreeding depression on a component vital rate (e.g., fecundity) and the effects of inbreeding depression on population growth underscores the importance of quantifying inbreeding costs relative to population dynamics to effectively manage endangered populations.