Role of inbreeding depression and purging in captive breeding and restoration programmes

Inbreeding depression is a major force affecting the evolution and viability of small populations in captive breeding and restoration programmes. Populations that experience small sizes may be less susceptible to future inbreeding depression because they have been purged of deleterious recessive alleles. We review issues related to purging, as they apply to the management of small populations, and discuss an experiment we conducted examining purging in populations of mosquitofish (Gambusia affinis). Purging is an important process in many small populations, but the literature contains a diversity of responses to purging both within and among studies. With the exception that slow inbreeding results in more purging and less threat to population viability, there seem to be few consistent trends that aid in prediction of how a purging event will affect a population. In our examination of purging on population viability in mosquitofish, single or multiple bottlenecks do not appear to have resulted in any purging of the influence of genetic load on population growth. Rather, serial bottlenecks resulted in a marked decline in population growth and an increase in extinction. Our results, taken together with those of reviewed studies, suggest that in small populations there is great uncertainty regarding the success of any single purging event in eliminating inbreeding depression, together with the high likelihood that purging will depress population viability through the fixation of deleterious alleles. In management of captive breeding and restoration programmes, the common practice of avoiding inbreeding and small population sizes should be followed whenever possible.     

DNA fingerprinting in Speke's gazelle: a test for genetic distinctness, and the correlation between relatedness and similarity

In the absence of pedigree information, the determination of genetic distinctness of populations can only be made by genetic methods. Using DNA fingerprinting on the North American captive herd of Speke's gazelle Gazella spekei , we were able to address two hypotheses. First, two new individuals were found to have come from a genetically distinct population ( P = 0.008, permutation test), and represent potential new founders to be added to the population. Secondly, genetic similarity was not significantly correlated with relatedness under extreme inbreeding and very close relationship (coefficient of relationship range 0.304-0.717).     

Seasonal stress drives predictable changes in inbreeding depression in field-tested captive populations of Drosophila melanogaster

Recent meta-analyses conducted across a broad range of taxa have demonstrated a strong linear relationship between the change in magnitude of inbreeding depression under stress and stress level, measured as fitness loss in outbred individuals. This suggests that a general underlying response may link stress and inbreeding depression. However, this relationship is based primarily on laboratory data, and it is unknown whether natural environments with multiple stressors and fluctuating stress levels alter how stress affects inbreeding depression. To test whether the same pattern persists in the field, we investigated the effect of seasonal variation on stress level and inbreeding depression in a 3-year field study measuring the productivity of captive populations of inbred and outbred Drosophila melanogaster. We found cold winter temperatures were most stressful and induced the greatest inbreeding depression. Furthermore, these data, collected under natural field conditions, conformed to the same predictive linear relationship seen in Drosophila laboratory studies, with inbreeding depression increasing by 0.17 lethal equivalents for every 10 per cent increase in stress level. Our results suggest that under natural conditions stress level is a primary determinant of the magnitude of inbreeding depression and should be considered when assessing extinction vulnerability in small populations.     

Reduced inbreeding depression in peripheral relative to central populations of a monocarpic herb

Many temperate taxa were confined to warmer latitudes during the last glacial maximum. As their ranges expanded when climates warmed, genetic drift and inbreeding in relatively small peripheral populations are expected to have reduced genetic diversity and the segregating genetic load. Therefore, inbreeding depression in peripheral populations might be lower than in centrally located sites. We evaluated the consequences of inbreeding for fitness traits in six central and six northern peripheral populations of the herb Campanulastrum americanum. Inbreeding reduced performance for all traits. Inbreeding depression in peripheral populations was lower than in central populations. This difference increased across the life cycle from similar levels for germination, to central populations having three times the inbreeding depression for adult traits. Geographical patterns of inbreeding depression suggest that mating system variation and potential future mating system evolution in many temperate taxa might reflect, at least in part, nonequilibrium conditions associated with historic range changes.     

Rapid genetic deterioration in captive populations: Causes and conservation implications

Many species require captive breeding to ensuretheir survival. The eventual aim of suchprograms is usually to reintroduce the speciesinto the wild. Populations in captivitydeteriorate due to inbreeding depression, lossof genetic diversity, accumulation of newdeleterious mutations and genetic adaptationsto captivity that are deleterious in the wild.However, there is little evidence on themagnitude of these problems. We evaluatedchanges in reproductive fitness in populationsof Drosophila maintained under benigncaptive conditions for 50 generations witheffective population sizes of 500 (2replicates), 250 (3), 100 (4), 50 (6) and 25(8). At generation 50, fitness in the benigncaptive conditions was reduced in smallpopulations due to inbreeding depression andincreased in some of the large populations dueto modest genetic adaptation. When thepopulations were moved to `wild' conditions,all 23 populations showed a marked decline(64–86%percnt;) in reproductive fitness compared tocontrols. Reproductive fitness showed acurvilinear relationship with population size,the largest and smallest population sizetreatments being the worst. Genetic analysesindicated that inbreeding depression andgenetic adaptation were responsible for thegenetic deterioration in `wild' fitness.Consequently, genetic deterioration incaptivity is likely to be a major problem whenlong-term captive bred populations ofendangered species are returned to the wild. Aregime involving fragmentation of captivepopulations of endangered species is suggestedto minimize the problems.     

Genetic rescue and inbreeding depression in Mexican wolves

Although inbreeding can reduce individual fitness and contribute to population extinction, gene flow between inbred but unrelated populations may overcome these effects. Among extant Mexican wolves (Canis lupus baileyi), inbreeding had reduced genetic diversity and potentially lowered fitness, and as a result, three unrelated captive wolf lineages were merged beginning in 1995. We examined the effect of inbreeding and the merging of the founding lineages on three fitness traits in the captive population and on litter size in the reintroduced population. We found little evidence of inbreeding depression among captive wolves of the founding lineages, but large fitness increases, genetic rescue, for all traits examined among F1 offspring of the founding lineages. In addition, we observed strong inbreeding depression among wolves descended from F1 wolves. These results suggest a high load of deleterious alleles in the McBride lineage, the largest of the founding lineages. In the wild, reintroduced population, there were large fitness differences between McBride wolves and wolves with ancestry from two or more lineages, again indicating a genetic rescue. The low litter and pack sizes observed in the wild population are consistent with this genetic load, but it appears that there is still potential to establish vigorous wild populations.     

Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population

Inbreeding is common in small and threatened populations and often has a negative effect on individual fitness and genetic diversity. Thus, inbreeding can be an important factor affecting the persistence of small populations. In this study, we investigated the effects of inbreeding on fitness in a small, wild population of house sparrows (Passer domesticus) on the island of Aldra, Norway. The population was founded in 1998 by four individuals (one female and three males). After the founder event, the adult population rapidly increased to about 30 individuals in 2001. At the same time, the mean inbreeding coefficient among adults increased from 0 to 0.04 by 2001 and thereafter fluctuated between 0.06 and 0.10, indicating a highly inbred population. We found a negative effect of inbreeding on lifetime reproductive success, which seemed to be mainly due to an effect of inbreeding on annual reproductive success. This resulted in selection against inbred females. However, the negative effect of inbreeding was less strong in males, suggesting that selection against inbred individuals is at least partly sex specific. To examine whether individuals avoided breeding with close relatives, we compared observed inbreeding and kinship coefficients in the population with those obtained from simulations of random mating. We found no significant differences between the two, indicating weak or absent inbreeding avoidance. We conclude that there was inbreeding depression in our population. Despite this, birds did not seem to actively avoid mating with close relatives, perhaps as a consequence of constraints on mating possibilities in such a small population.     

No evidence of inbreeding avoidance or inbreeding depression in a social carnivore

Dispersal by young mammals away from their natal site is generallythought to reduce inbreeding, with its attendant negative fitnessconsequences. Genetic data from the dwarf mongoose, a pack-livingcarnivore common in African savannas, indicate that there areexceptions to this generalization. In dwarf mongoose populationsin the Serengeti National Park, Tanzania, breeding pairs arecommonly related, and close inbreeding has no measurable effecton offspring production or adult survival. Inbreeding occursbecause average relatedness among potential mates within a packis high, because mating patterns within the pack are randomwith respect to the relatedness of mates, and because dispersaldoes little to decrease the relatedness among mates. Young femalesare more likely to leave a pack when the dominant male is aclose relative but are relatively infrequent dispersers. Youngmales emigrate at random with respect to the relatedness ofthe dominant female and tend to disperse to packs that containgenetically similar individuals.[Behav Ecol 7: 480–489(1996)]     

An analytical investigation of the dynamics of inbreeding in multi-generation supportive breeding

Supportive breeding is being increasingly usedas a measure to reduce the short-termprobability of extinction of populations withhighly reduced abundance relative to historicallevels. In this paper, we provide a conceptualframework and analytical tools to computechanges in inbreeding coefficient (F) in thecase of supportive breeding over any number ofgenerations. The dynamics of inbreedingcoefficients were investigated by means of asystem of recurrence equations. We focussed onquantifying the dynamics of F for specificcombinations of parameter values in terms ofthe effects of captive population census size,refreshment rate of breeders in captivity,scale of supplementation program, and migrationrate. We observed that supplementation did notalways result in substantial inbreedingincrement and several conditions loweredoverall inbreeding relative to controlsituations without supplementation. The censussize of captive populations was the single mostimportant controllable parameter determiningthe genetic consequences of supportivebreeding. While the proportion of captivebreeders brought into captivity from the wildbore a complex relationship to inbreedingcoefficient dynamics, the results indicatedthat managers should generally aim at highrefreshment rates (that is, large proportionsof their captive stock originating from thewild). This is especially important when asmall captive population is expected tocontribute large numbers of breeders to thesupplemented population. The analysis alsoshowed how supplemented populations connectedto a large metapopulation through gene flowrecover from the genetic risks of inbreedingdue to supportive breeding program more quicklythan isolated populations. The results of thisstudy join those of an increasing number ofinvestigations showing that supportive breedingdoes not always increase inbreeding, and mayeven decrease it in several circumstances.However, supportive breeding systems arecomplex, and results such as presented hereshould not be used in isolation, but inconsideration of other issues such as theconsequences on long-term fitness of wildindividuals.     

Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging

An important issue in conservation biology and the study of evolution is the extent to which inbreeding depression can be reduced or reversed by natural selection. If the deleterious recessive alleles causing inbreeding depression can be 'purged' by natural selection, outbred populations that have a history of inbreeding are expected to be less susceptible to inbreeding depression. This expectation, however, has not been realized in previous laboratory experiments. In the present study, we used Drosophila melanogaster as a model system to test for an association between inbreeding history and inbreeding depression. We created six 'purged' populations from experimental lineages that had been maintained at a population size of 10 male-female pairs for 19 generations. We then measured the inbreeding depression that resulted from one generation of full-sib mating in the purged populations and in the original base population. The magnitude of inbreeding depression in the purged populations was approximately one-third of that observed in the original base population. In contrast to previous laboratory experiments, therefore, we found that inbreeding depression was reduced in populations that have a history of inbreeding. The large purging effects observed in this study may be attributable to the rate of historical inbreeding examined, which was slower than that considered in previous experiments.     

Modeling problems in conservation genetics using captive Drosophila populations: Improvement of reproductive fitness due to immigration of one individual into small partially inbred populations

Immigration into small isolated captive and wild populations is recommended to alleviate inbreeding depression. The effects on reproductive fitness of introducing one immigrant into 10 small partially inbred captive populations of D. melanogaster were evaluated. The relative reproductive fitness of the immigrant populations (0.628) was approximately double that of the isolated populations (0.294) and about halfway between the isolated populations and the outbred base population (1.00). Every replicate population increased in fitness following the introduction of an immigrant. The improvements in reproductive fitness shown by the immigrant populations were not due to F₁ hybrid vigor, as the experimental populations underwent three generations of random mating prior to the fitness tests. These results indicate substantial benefits can be gained by the translocation of as few as a single animal between small, partially inbred populations. © 1992 Wiley-Liss, Inc.     

Strategies for maintaining genetic diversity in captive populations through reproductive technology

The maintenance of genetic diversity in captive populations is a primary goal of captive breeding plans, and it is becoming increasingly apparent that reproductive technology has much to offer captive breeding programs in attaining this goal. Reproductive technology can best assist captive breeding programs in this task by developing strategies that effectively increase the genetic contribution of new wild founders to a population as well as increase the reproductive life span of existing founders and their close descendents. This will act to reduce genetic drift and inbreeding effects in the population and thereby minimize the loss of genetic diversity. Considering only one aspect of reproductive technology, semen collection, this paper examines some of the genetic considerations that might be used for choosing which males in a population to collect semen from, assuming the goal of the captive breeding program is the preservation of genetic diversity. It is shown that semen collection and preservation, with future intent of artificial insemination, can make significant contributions to the maintenance of genetic diversity if careful consideration is given to the selection of donor males. Finally, the pedigree of the captive population of Asian lions (Panthera leo persica) is used to illustrate some of these genetic concepts that might be important in selecting males as semen donors.     

Inbreeding depression in Lychnis flos-cuculi (Caryophyllaceae): effects of different levels of inbreeding

In a controlled crossing experiment on Lychnis flos-cuculi plants in the greenhouse, outbred and selfed maternal plants were each treated with pollen from unrelated plants, siblings and selves. The seeds thus obtained had expected inbreeding coefficients of 0, 0.25 and 0.5 for the outbred maternal plants, and 0, 0.5 and 0.75 for the selfed maternal plants. Seed abortion rate, seed weight and germination rate were estimated. Seedlings were transplanted to an outdoor garden, and monitored for survival, probability of flowering, number of capsules and area of capsules next spring. Inbred seeds germinated slower and in lower proportions than those less inbred, and seedlings had lower survival, flowering, fruit set and area of capsules if inbred. Combined fitness values were estimated from the survival and fecundity components, and severe inbreeding depression was detected for these estimates (0.51 and 0.56 for one generation of selfing). The fitness function decreased linearly with the increase in inbreeding coefficient, which is as expected if the inbreeding depression is additive among loci.     

Effect of inbreeding depression on outcrossing rates among populations of a tropical pine

Inbreeding depression is common among plants and may distort mating system estimates. Mating system studies traditionally ignore this effect, nonetheless an assessment of inbreeding depression that may have occurred before progeny evaluation could be necessary. In the neotropical Pinus chiapensis inbreeding depression was evaluated using regression analysis relating progeny F-values with seed germinability, the mating system was analysed in three populations with contrasting size, using isozymes, obtained a corrected outcrossing rate. Selfing decreased seed viability by 19%, relative to an outcrossed plant. Multilocus outcrossing rates, t(m), varied widely among populations. In the two smallest populations t(m) congruent with 1. Therefore, inbreeding depression did not affect the estimates, but overestimated t(m) by 10% in the third population, which has a true mixed mating system (selfing was the major source of inbreeding), and an unusually low t(m) for pines (t(m) = 0.54, uncorrected, t(m) = 0.49, corrected). Inbreeding depression may be an uneven source of bias for outcrossing estimates even at the infraspecific level. Accuracy [corrected] but not precision [corrected] may be gained by including inbreeding depression in outcrossing estimates. Therefore, caution should be taken when comparing t(m) among species or even populations within the same species.     

Family level inbreeding depression and the evolution of plant mating systems

Variation in the magnitude of inbreeding depression (ID) among families may have important consequences for mating system evolution. Experimental studies have shown that such variation is a common feature of natural plant populations. Unfortunately, the genetic and evolutionary significance of family level estimates remains obscure. Almost any kind of genetic variation will generate differences in ID among families, and as a consequence, a non-zero variance in family level ID is not sufficient to distinguish genetic architectures with wholly different implications for mating system evolution. Quantitative genetic methods provide a means to extract more information from ID experiments. Estimates of quantitative genetic variance components directly inform questions about the genetic basis of ID and should ultimately allow tests of alternative theories of mating system evolution.     

Modeling problems in conservation genetics using captive Drosophila populations: Consequences of equalizing founder representation

Equalizing founder representation is a recommended practice for maintaining captive populations. However, this procedure has not been subject to controlled experimental evaluation. The effects on inbreeding, genetic variation, and reproductive fitness of maintaining small captive populations by equalizing founder representation (EFR) versus randomly choosing parents (RC) were compared. Ten replicate lines were created with unequal founder representations, split into EFR and RC lines, and maintained for a further eight generations. Founder representations computed from pedigrees were closer to equality in the EFR lines than in the RC lines or the base population, most of the changes being evident after one generation. Significant benefits of EFR were found in lowered inbreeding (mean inbreeding coefficients of 0.35 and 0.41, respectively, for EFR and RC lines) and average heterozygosity (0.141 for EFR, 0.084 for RC, compared with 0.216 in the base population). However, EFR was not significantly better than RC in moving allele frequencies towards equalized founder representation. No significant difference was found in reproductive fitness between EFR and RC (relative fitnesses compared to the base population were 0.179 for EFR and 0.182 for RC). The use of equalization of founder representation for a few generations can be recommended in the genetic management of captive populations derived from a small number of founders that contribute unequally. © 1992 Wiley-Liss, Inc.     

Characterization of eight microsatellite loci in Grant's gazelle (Gazella granti)

Eight microsatellite loci were isolated from a genomic DNA library created from Grant's gazelle (Gazella granti). Observed and expected levels of heterozygosity were computed utilizing 20 individuals from a population in Central Kenya. Tests for Hardy–Weinberg equilibria were conducted and found that two of the eight loci deviated from equilibrium in this population. These markers were developed to analyse the genetic effects of culling and isolation on a game preserve in Kenya.     

Multilocus heterozygosity and inbreeding depression in an insular house sparrow metapopulation

Inbreeding causes reduction of genetic variability that may have severe fitness consequences. In spite of its potentially huge impact on viability and evolutionary processes especially in small populations, quantitative demonstrations of genetic and demographic effects of inbreeding in natural populations are few. Here, we examine the relationship between individual inbreeding coefficients (F) and individual standardized multilocus heterozygosity (H) in an insular metapopulation of house sparrows (Passer domesticus) in northern Norway in order to evaluate whether H is a good predictor for F. We then relate variation in fitness (i.e. the probability of surviving from fledging to recruitment) to F and H, which enables us to examine whether inbreeding depression is associated with a reduction in genetic variability. The average level of inbreeding in the house sparrow metapopulation was high, and there was large inter-individual variation in F. As expected, standardized multilocus heterozygosity decreased with the level of inbreeding. The probability of recruitment was significantly negatively related to F, and, accordingly, increased with H. However, H explained no significant additional variation in recruitment rate than was explained by F. This suggests that H is a good predictor for F in this metapopulation, and that an increase in F is likely to be associated with a general increase in the level of homozygosity on loci across the genome, which has severe fitness consequences.