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.     

Relationship between Population Size and Fitness

Abstract:  Long-term effective population size, which determines rates of inbreeding, is correlated with population fitness. Fitness, in turn, influences population persistence. I synthesized data from the literature concerning the effects of population size on population fitness in natural populations of plants to determine how large populations must be to maintain levels of fitness that will provide adequate protection against environmental perturbations that can cause extinction. Integral to this comment on what has been done and what needs to be done, sThe evidence suggests that there is a linear relationship between log population size and population fitness over the range of population sizes examined. More importantly, populations will have to be maintained at sizes of >2000 individuals to maintain population fitness at levels compatible with the conservation goal of long-term persistence. This approach to estimating minimum viable population size provides estimates that are in general agreement with those from numerous other studies and strengthens the argument that conservation efforts should ultimately aim at maintaining populations of several thousand individuals to ensure long-term persistence.     

Is Mutation Accumulation a Threat to the Survival of Endangered Populations?

The accumulation of new deleterious mutations has been predicted to constitute a significant threat to the survival of finite sexually reproducing populations. Three measures of genetic load were made on populations of Drosophila melanogaster maintained at effective population sizes of 25, 50, 100, 250, and 500 for 45 or 50 generations and their outbred base population and a new sample from the same wild population. Genetic loads were measured as fitness differentials between inbred and non-inbred lines derived from each population under both benign ( productivity of single pairs) and competitive (competitive index) conditions. No trend of smaller populations exhibiting greater genetic loads than larger ones was observed under either benign or competitive conditions. Further, genetic loads were similar in captive and wild populations. Frequencies of deleterious and lethal alleles on chromosome II were measured by making the chromosome (approximately 40% of the genome) homozygous using a marked balancer stock. Neither deleterious nor lethal allele frequencies exhibited a relationship with population size. The accumulation of detrimental mutations does not appear to pose a significant threat to finite sexual populations with effective sizes of 25 or more over the 100–200 year time frames considered in most wildlife conservation programs.     

General and specific combining abilities of larval and juvenile growth and viability estimated from natural oyster populations

Diallel crosses of oysters from three geographically isolated natural populations were produced to evaluate the relative importance of genetic, maternal, and environmental effects on larval and juvenile growth and viability. Significant additive genetic effects were observed only in larval viability at Day 12 and larval shell length at Day 2. The presence of significant male and female mean square for larval viability (suggesting non-additive genetic variance) is consistent with fitness related characters. Important maternal effects were observed for the larval and juvenile shell length and viability characters. These female mean squares are probably affected by both real and spurious maternal effects and potential contributing influences are discussed. The performance of the crosses can be largely explained by two factors: parental performance and the heterotic gene effects. This is based on an apparent positive correlation of mean values between the parental populations and their crosses. The crosses' mean viability at the end of the larval phase was 14.0% lower than the pure matings and support a previous observation of lower heterozygote viability in the larval phase (Mallet and Haley, 1983b).     

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.     

Double Allee Effects and Extinction in the Island Fox

Abstract:  An Allee effect (AE) occurs in populations when individuals suffer a decrease in fitness at low densities. If a fitness component is reduced (component AE), per capita population growth rates may decline as a consequence (demographic AE) and extinction risk is increased. The island fox ( Urocyon littoralis ) is endemic to six of the eight California Channel Islands. Population crashes have coincided with an increase in predation by Golden Eagles ( Aquila chrysaetos ). We propose that AEs could render fox populations more sensitive and may be a likely explanation for their sharp decline. We analyzed demographic data collected between 1988 and 2000 to test whether fox density (1) influences survival and reproductive rates; (2) interacts with eagle presence and affects fox fitness parameters; and (3) influences per capita fox population trends. A double component AE simultaneously influenced survival (of adults and pups) and proportion of breeding adult females. The adult survival AE was driven by predation by eagles. These component AEs led to a demographic AE. Multiple-component AEs, a predation-driven AE, and the simultaneous occurrence of both component and demographic AEs in a mammal are all previously unreported processes. Populations below 7 foxes/km² could have suboptimal population growth rates due to the demographic AE, and AEs may have contributed to the dramatic declines in three fox populations. Because fox densities in critically endangered populations are well below this level, removing Golden Eagles appears necessary to prevent a predation-driven AE. Conservationists should also be aware of AEs when planning the release of captive foxes. More generally, our findings highlight the danger of overlooking AEs in the conservation of populations of rare or threatened species.     

Genetic and demographic consequences of importing animals into a small population: a simulation model of the Texas State Bison Herd (USA)

The extant 40 bison (Bison bison) constituting the Texas State Bison Herd (TSBH; USA) are directly and exclusively descended from a bison herd assembled by Charles Goodnight in the 1880s, representing a historically and genetically valuable resource. The population currently suffers from low genetic variation, low heterozygosity, high calf mortality, and low natality rates compared with other closed bison populations. Population viability analysis using the VORTEX program previously indicated a 99% chance of population extinction within the next 41 years [J. Mamm. 85 (2004) in press]. We developed a stochastic simulation model to evaluate the genetic and demographic consequences of various management scenarios for the TSBH using genotypic data from 51 microsatellite loci and demographic information recorded over a 6-year period. Our results reveal that without the introduction of new genetic variation, approximately 37% of the representative microsatellite loci will become fixed as the TSBH continues to lose genetic variation at a staggering rate of 30–40% within the next 50 years. Furthermore, if the current trends in natality and mortality rates continue, our model indicates the TSBH faces a 99% chance of extinction in the next 51 years. With the importation of unrelated male bison into the TSBH, and under the assumption of increased fitness, the probability of population survival in the next 100 years increases to 100%, and the population will reach the approximate carrying capacity of 200 bison in 15–16 years. Furthermore, our model predicts increases in genetic diversity and heterozygosity of 24.7–48.4% and 17.5–36.5%, respectively, in the next 100 years following the addition of new genetic variation. We conclude that the importation of bison into the TSBH is necessary to prevent extinction and ensure long-term population survival.     

Natural Die-Offs of Large Mammals: Implications for Conservation

The viability of populations is a central concern of biological conservation. The occurrence of catastrophic die-offs may greatly reduce the long-term viability of populations. Theoretical extinction models and viability analyses require information on the frequency of die-offs and on the distribution of die-off severities. A review of literature identified 96 natural die-offs in large mammal populations, with a die-off being defined as a peak-to-trough decline in estimated population numbers of at least 25%. If such die-offs are common, population viability analyses that ignore them may be overly optimistic. The severities of the natural die-offs of large mammals presented here are not uniformly distributed. There is a relative overabundance of die-offs in the 70–90% range, and an underabundance of die-offs greater than 90%. This may indicate the presence of buffers against population extinction. The reported causes of large mammal die-offs were significantly related to trophic level: herbivore die-offs were more often attributed to starvation, while carnivore die-offs were more often attributed to disease. Populations subject to large-scale phenomena such as drought and severe winters may not be protected from die-offs by population subdivision. On the other hand, populations subject to catastrophic disease epidemics may be protected by subdivision, and threatened by corridors between conservation areas and by translocation efforts.     

Competition with flies promotes communal breeding in the burying beetle,Nicrophorus tomentosus

Communal breeding through nest-sharing may benefit cooperating individuals indirectly, in increased inclusive fitness, or directly, when environmental constraints reduce the fitness of solitary breeders. Burying beetles provide extensive parental care and can breed either in pairs or in larger groups of unrelated males and females. Parentage of communally-reared broods is usually shared but is skewed in favor of the individuals of each sex that provide longer care. Females provide care longer than males, and two females are more likely to remain together in the brood chamber than two males are. Flies and other burying beetles are the major competitors for carcasses and this study suggests that it is competition with flies that promotes communal breeding inNicrophorus tomentosus On medium-size carcasses (35–40 g) the presence or absence of oviposition by flies had a significant effect on the size of the brood reared, and on large carcasses (55–60 g) the number of beetles present, two or four, had a significant effect on brood size. On both medium and large carcasses, pairs rearing broods on flyblown carcasses had fewer young than pairs on clean carcasses or foursomes on flyblown carcasses. There was a strong trend for an interaction effect between number of beetles and competition with flies (Table 1). Duration of parental care was not affected by competition with flies except for that of the first male to depart, which provided care longer on flyblown carcasses (Table 2). Pairs and foursomes were equally able to defend the carcass and brood from conspecific intruders and from larger intrudingNicrophorus orbicollis (Table 3).     

Fitness Decline under Relaxed Selection in Captive Populations

Abstract: We compared life-history schedules among populations of the housefly (  Musca domestica L.) maintained in the laboratory under curtailed life span, such that selection on mutations that affected only late-life fitness traits was reduced. As a result of this regime, late-life ( but not early-life) fecundity declined within a few generations. The results suggest that if captive populations are maintained with minimal selection, either by direct manipulation of the environment or by equalizing family contributions, the increased frequency of potentially deleterious mutations may rapidly lower the ability of these populations to exist under natural conditions. This would be independent of population size, so expanding captive populations would not alleviate potential fitness reductions due to relaxed selection.     

Unprecedented Low Levels of Genetic Variation and Inbreeding Depression in an Island Population of the Black-Footed Rock-Wallaby

Abstract: It has been argued that demographic and environmental factors will cause small, isolated populations to become extinct before genetic factors have a significant negative impact. Islands provide an ideal opportunity to test this hypothesis because they often support small, isolated populations that are highly vulnerable to extinction. To assess the potential negative impact of isolation and small population size, we compared levels of genetic variation and fitness in island and mainland populations of the black-footed rock-wallaby ( Petrogale lateralis [Marsupialia: Macropodidae]). Our results indicate that the Barrow Island population of P. lateralis has unprecedented low levels of genetic variation (  H _e = 0.053, from 10 microsatellite loci) and suffers from inbreeding depression (reduced female fecundity, skewed sex ratio, increased levels of fluctuating asymmetry). Despite a long period of isolation ( ∼ 1600 generations) and small effective population size (  N _e ∼ 15), demographic and environmental factors have not yet driven this population to extinction. Nevertheless, it has been affected significantly by genetic factors. It has lost most of its genetic variation and become highly inbred (  F _e = 0.91), and it exhibits reduced fitness. Because several other island populations of P. lateralis also exhibit exceptionally low levels of genetic variation, this phenomenon may be widespread. Inbreeding in these populations is at a level associated with high rates of extinction in populations of domestic and laboratory species. Genetic factors cannot then be excluded as contributing to the extinction proneness of small, isolated populations.     

Gene Flow and Genetic Restoration: The Florida Panther as a Case Study

Populations of some endangered species have become so small that they have lost genetic variation and appear to have become fixed for deleterious genetic variants. To avoid extinction from this genetic deterioration individuals from related subspecies or populations may have to be introduced for genetic restoration i.e., elimination of deleterious variants and recovery to a normal level of genetic variation. I construct a general population genetics framework from which to evaluate the potential for genetic restoration, and I discuss its specific application to the Florida panther. The translocation of Texas cougars into the free-ranging Florida panther population has been recommended to genetically restore the Florida panther, a subspecies of Felis concolor that appears to have both a low level of genetic variation and low fitness. Specific recommendations recently given by a scientific panel are to introduce enough animals so that there is approximately 20% gene flow in the first generation of translocation and approximately 2–4% in the generations thereafter. I evaluated these recommendations in a theoretical population genetics framework and found that they should result in the removal of most detrimental genetic variation and an increase in the standing genetic variation without a high probability of loss of any adaptive Florida panther alleles. Unless the population of the free-ranging Florida panthers is very small, the planned translocation should result in genetic restoration of the Florida panther.     

Increased Infectious Disease Susceptibility Resulting from Outbreeding Depression

Abstract:  The mechanisms by which outbreeding depression leads to reduced fitness are poorly understood. We considered the hypothesis that outbreeding can depress fitness by increasing the susceptibility of hybrid individuals and populations to infectious disease. Competitive breeding trials in experimental ponds indicated that outbred largemouth bass (  Micropterus salmoides ) crossed from two geographically and genetically distinct populations suffered a reduction in fitness of approximately 14% relative to parental stocks. We measured the comparative susceptibility of these same outbred stocks to a novel viral pathogen, largemouth bass virus. Following experimental inoculation, F2 generation hybrids suffered mortality at a rate 3.6 times higher than either F1 generation hybrids or wild-type parental fish. Analysis of viral loads indicated that viral replication was more rapid in F2 fish than in F1 hybrids or wild-type parental fish. We attribute these results to the disruption of coadapted gene complexes in the immune systems of outbred fish in the F2 generation. Increased susceptibility to infectious disease may be an important but underappreciated mechanism by which outbreeding reduces the fitness of individuals and populations and by which novel infectious diseases emerge in populations of hybrid organisms.     

Releasing Adults versus Young in Reintroductions: Interactions between Demography and Genetics

Abstract:  We integrated genetics and demography into population modeling in the context of species restorations, in which both the origin of released individuals and the management strategy may influence the success of introduction. Through an explicit individual-based simulation approach, we investigated the effects of the age of released individuals by exploring the relative merits of releasing juveniles or adults to establish populations. We included the effect of genetic variability responsible for inbreeding depression and mutational meltdown. Our general analysis uncovered an interaction between the age of founders and the extent of intrapopulation fitness variability, which substantially influenced the efficiency of selection in populations founded by juveniles and had subsequent positive consequences for long-term persistence compared with the case in which adults were released. We then applied the model to the case of the reintroduction of the Griffon Vulture ( Gyps fulvus fulvus ) to southern France, for which post-release data were available. The demographic aspects of this reintroduction were already analyzed and published, suggesting that it is more efficient to release adults than juveniles, despite an observed reduction of demographic parameters following the release of adults. In that context, the inclusion of genetic considerations qualitatively changes the conclusion, predicting reduced long-term extinction risk if juveniles rather than adults are released.     

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.     

Predicting the Deleterious Effects of Mutation Load in Fragmented Populations

Abstract:  Human-induced habitat fragmentation constitutes a major threat to biodiversity. Both genetic and demographic factors combine to drive small and isolated populations into extinction vortices. Nevertheless, the deleterious effects of inbreeding and drift load may depend on population structure, migration patterns, and mating systems and are difficult to predict in the absence of crossing experiments. We performed stochastic individual-based simulations aimed at predicting the effects of deleterious mutations on population fitness (offspring viability and median time to extinction) under a variety of settings (landscape configurations, migration models, and mating systems) on the basis of easy-to-collect demographic and genetic information. Pooling all simulations, a large part (70%) of variance in offspring viability was explained by a combination of genetic structure ( F_ST ) and within-deme heterozygosity ( H_S ). A similar part of variance in median time to extinction was explained by a combination of local population size ( N ) and heterozygosity ( H_S ). In both cases the predictive power increased above 80% when information on mating systems was available. These results provide robust predictive models to evaluate the viability prospects of fragmented populations.     

Evidence of large-scale source-sink dynamics and long-distance dispersal among Wood Thrush populations

Source-sink dynamics are commonly thought to occur among Wood Thrush (Hylocichla mustelina) and other songbird populations, allowing for the persistence of populations with negative growth rates ("sinks") through immigration from populations with positive growth rates ("sources"). Knowledge of source-sink dynamics is important for management and conservation because the removal of source habitat should result in the extinction of dependent sinks. However, since research has focused on identifying individual sources/sink populations, not source-sink pairs, we cannot predict these effects or the scale over which they occur. We posit that, when dispersal occurs from a source to a sink year after year, there will be a one-year time-lagged correlation in abundance between the two populations. This should occur for populations separated by distances over which juveniles disperse. Using the North American Breeding Bird Survey data, we tested for such time-lagged correlations between paired Wood Thrush populations from 10 to 200 km apart. Populations were linked with a one-year time lag over distances from 60 to 80 km, indicating that dispersal and source-sink dynamics may occur over these long distances. There was also a declining trend in forest cover from sources to sinks. Conservation and management strategies should therefore be designed at large scales, with consideration for source-sink dynamics and forest cover.     

Long-Term Population Changes of Native and Introduced Birds in the Alaka'i Swamp, Kaua'i

Abstract:  Within the last 30 years, five endemic bird species of the Alaka'i Swamp, Kaua'i, Hawai'i, have likely gone extinct. We documented population trends of the remaining avifauna in this time period to identify a common pattern in the Hawaiian Islands: decline of native species and expansion of introduced species. We conducted bird surveys over 100 km² of the Alaka'i and Kōke'e regions of Kaua'i in March–April 2000 to estimate population size, distribution, and range limits of seven native and six introduced forest birds. We compared the results with four previous surveys conducted over the last 30 years. Five of the seven native species we studied have fared well, maintaining sizeable populations (>20,000 individuals) and unchanged or increasing numbers. The endemic 'Akikiki ( Oreomystis bairdi ), however, declined from 6296 (SE ± 1374) to 1472 (SE ± 680) individuals and exhibited range contraction from 88 to 36 km². The 'I'iwi ( Vestiaria coccinea ) also experienced a decline and contraction, though not as severe. Populations of several introduced forest birds are increasing, but all species, excluding the Japanese White-eye ( Zosterops japonicus ), were at low numbers (<5,500 individuals in survey area). One introduced species, the Japanese Bush-Warbler ( Cettia diphone ) recently invaded, whereas another, the Red-billed Leiothrix ( Leiothrix lutea ), has been extirpated. Two hurricanes in the past 20 years appear to have most strongly affected nectarivores and may have contributed to the decline or extinction of several other species. Overall, native bird populations on Kaua'i have exhibited species-specific responses to limiting factors. Although most native populations appear stable, the extant native avifauna is vulnerable as a result of limited distributions and the potential for widespread habitat degradation.     

Influence of habitat quality, population size, patch size, and connectivity on patch-occupancy dynamics of the middle spotted woodpecker

Despite extensive research on the effects of habitat fragmentation, the ecological mechanisms underlying colonization and extinction processes are poorly known, but knowledge of these mechanisms is essential to understanding the distribution and persistence of populations in fragmented habitats. We examined these mechanisms through multiseason occupancy models that elucidated patch-occupancy dynamics of Middle Spotted Woodpeckers (Dendrocopos medius) in northwestern Spain. The number of occupied patches was relatively stable from 2000 to 2010 (15-24% of 101 patches occupied every year) because extinction was balanced by recolonization. Larger and higher quality patches (i.e., higher density of oaks >37 cm dbh [diameter at breast height]) were more likely to be occupied. Habitat quality (i.e., density of large oaks) explained more variation in patch colonization and extinction than did patch size and connectivity, which were both weakly associated with probabilities of turnover. Patches of higher quality were more likely to be colonized than patches of lower quality. Populations in high-quality patches were less likely to become extinct. In addition, extinction in a patch was strongly associated with local population size but not with patch size, which means the latter may not be a good surrogate of population size in assessments of extinction probability. Our results suggest that habitat quality may be a primary driver of patch-occupancy dynamics and may increase the accuracy of models of population survival. We encourage comparisons of competing models that assess occupancy, colonization, and extinction probabilities in a single analytical framework (e.g., dynamic occupancy models) so as to shed light on the association of habitat quality and patch geometry with colonization and extinction processes in different settings and species.     

Simulation of the Effect of Spatial and Temporal Variation in Fire Regimes on the Population Viability of a Banksia Species

Populations of plants that rely on seeds for recovery from disturbance by fire (obligate seeders) are sensitive to regimes of frequent fire. Obligate seeders are prominent in fire-prone heathlands of southern Australia and South Africa. Population extinction may occur if there are successive fires during a plant's juvenile period. Research on the population biology of obligate seeders has influenced the management of fire in these heath and shrublands, but work on the effects of the spatial variability of fires is lacking. We hypothesize that extinction maybe avoided under an adverse fire frequency if fires are patchy. We present a model that simulates the effects of spatial and temporal variations in fire regimes on the viability of a plant population in a grid landscape. Seedling establishment, maturation, senescence, and seed dispersal determine the presence or absence of plants in each cell. We used values typical of serotinous Banksia species to estimate probability of extinction in relation to fire frequency and size. We examined the sensitivity of predictions to dispersal, senescence, fire frequency, spatial burning pattern and size variance, and the size of the grid. Simulations 200 years in length indicated that extinction probability was lowest when mean fire frequency was intermediate and mean fire size was large. When fire frequency was high, extinction probability was high irrespective of fire size. Senescence was more important than high-frequency fire as a cause of extinction in cells. Interactions between dispersal, fire frequency, and size were complex, indicating that extinction is governed by intercell connectivity. The model indicates that fire patchiness cannot be assumed to ensure avoidance of extinction of populations. Conservation of populations is most likely when fire patchiness is relatively low—when the size of fires is moderate to large and when burned patches are contiguous.