Inbreeding In Small Populations Research Articles

Genomic approaches to mitigating genetic diversity loss in declining populations.

The accelerating pace of global biodiversity loss is exacerbated by habitat fragmentation and subsequent inbreeding in small populations. To address this problem, conservation practitioners often turn to assisted breeding programmes with the aim of enhancing genetic diversity in declining populations. Although genomic information is infrequently included in these efforts, it has the potential to significantly enhance the success of such programmes. In this study, we showcase the value of genomic approaches for increasing genetic diversity in assisted breeding efforts, specifically focusing on a highly inbred population of Western burrowing owls. To maximize genetic diversity in the resulting offspring, we begin by creating an optimal pairing decision tree based on sex, kinship and patterns of homozygosity across the genome. To evaluate the effectiveness of our strategy, we compare genetic diversity, brood size and nestling success rates between optimized and non-optimized pairs. Additionally, we leverage recently discovered correlations between telomere length and fitness across species to investigate whether genomic optimization could have long-term fitness benefits. Our results indicate that pairing individuals with contrasting patterns of homozygosity across the genome is an effective way to increase genetic diversity in offspring. Although short-term field-based metrics of success did not differ significantly between optimized and non-optimized pairs, offspring from optimized pairs had significantly longer telomeres, suggesting that genetic optimization can help reduce the risk of inbreeding depression. These findings underscore the importance of genomic tools for informing efforts to preserve the adaptive potential of small, inbred populations at risk of further decline.

"Type D" killer whale genomes reveal long-term small population size and low genetic diversity.

Genome sequences can reveal the extent of inbreeding in small populations. Here, we present the first genomic characterization of type D killer whales, a distinctive eco/morphotype with a circumpolar, subantarctic distribution. Effective population size is the lowest estimated from any killer whale genome and indicates a severe population bottleneck. Consequently, type D genomes show among the highest level of inbreeding reported for any mammalian species (FROH ≥ 0.65). Detected recombination cross-over events of different haplotypes are up to an order of magnitude rarer than in other killer whale genomes studied to date. Comparison of genomic data from a museum specimen of a type D killer whale that stranded in New Zealand in 1955, with 3 modern genomes from the Cape Horn area, reveals high covariance and identity-by-state of alleles, suggesting these genomic characteristics and demographic history are shared among geographically dispersed social groups within this morphotype. Limitations to the insights gained in this study stem from the nonindependence of the 3 closely related modern genomes, the recent coalescence time of most variation within the genomes, and the nonequilibrium population history which violates the assumptions of many model-based methods. Long-range linkage disequilibrium and extensive runs of homozygosity found in type D genomes provide the potential basis for both the distinctive morphology, and the coupling of genetic barriers to gene flow with other killer whale populations.

Negative effect of inbreeding on fitness of an arctic–alpine Hieracium alpinum (Asteraceae), a species with a geographical parthenogenesis distribution pattern

Decreased fitness due to inbreeding in small populations can be a considerable disadvantage in sexually reproducing organisms compared to their asexual relatives. Therefore, inbreeding depression of sexuals could contribute to geographical parthenogenesis (GP) distribution patterns, when sexuals have more restricted distribution than their asexual relatives. In this study, we tested whether biparental inbreeding will lead to decreased fitness in sexual diploids of Hieracium alpinum, a species showing a GP distribution pattern. We performed three types of crosses (inbred, outbred, and interpopulation outbred) and measured eleven fitness traits. A subset of plants was also grown with a natural competitor Nardus stricta to increase any negative effects of inbreeding. We found significant effects of inbreeding in two out of eleven measured traits in the F1 generation. Initial biomass was statistically significantly lower by 9.6% in inbred lineages compared to outbred lineages. Similar trends, i.e., lower values in inbred progeny when compared to outbred one, were found also in final biomass and survival rate (values decreased in inbred progeny by 17.5% and 11.5%, respectively), but these differences were statistically nonsignificant. However, the negative effect of inbreeding on these traits was not increased by the presence of Nardus stricta as a competitor. Our results suggest that biparental inbreeding could to some extent explain a lowered colonizing ability of sexual diploid of H. alpinum, but the GP pattern observed is also likely to be influenced by other processes and their interactions.

Evolutionary principles guiding amphibian conservation.

The Anthropocene has witnessed catastrophic amphibian declines across the globe. A multitude of new, primarily human‐induced drivers of decline may lead to extinction, but can also push species onto novel evolutionary trajectories. If these are recognized by amphibian biologists, they can be engaged in conservation actions. Here, we summarize how principles stemming from evolutionary concepts have been applied for conservation purposes, and address emerging ideas at the vanguard of amphibian conservation science. In particular, we examine the consequences of increased drift and inbreeding in small populations and their implications for practical conservation. We then review studies of connectivity between populations at the landscape level, which have emphasized the limiting influence of anthropogenic structures and degraded habitat on genetic cohesion. The rapid pace of environmental changes leads to the central question of whether amphibian populations can cope either by adapting to new conditions or by shifting their ranges. We gloomily conclude that extinction seems far more likely than adaptation or range shifts for most species. That said, conservation strategies employing evolutionary principles, such as selective breeding, introduction of adaptive variants through translocations, ecosystem interventions aimed at decreasing phenotype–environment mismatch, or genetic engineering, may effectively counter amphibian decline in some areas or for some species. The spread of invasive species and infectious diseases has often had disastrous consequences, but has also provided some premier examples of rapid evolution with conservation implications. Much can be done in terms of setting aside valuable amphibian habitat that should encompass both natural and agricultural areas, as well as designing protected areas to maximize the phylogenetic and functional diversity of the amphibian community. We conclude that an explicit consideration and application of evolutionary principles, although certainly not a silver bullet, should increase effectiveness of amphibian conservation in both the short and long term.

Conservation: The Costs of Inbreeding and of Being Inbred.

Endangered species face a huge array of challenges, including the negative consequences of individuals having to breed with close genetic relatives. But just how costly is inbreeding in small populations? New research from an endangered bird species suggests that considering inbreeding could be crucial for conservation programmes.

Temporal trends in genetic data and effective population size support efficacy of management practices in critically endangered dusky gopher frogs (Lithobates sevosus).

Monitoring temporal changes in population genetic diversity and effective population size can provide vital information on future viability. The dusky gopher frog, Lithobates sevosus, is a critically endangered species found only in coastal Mississippi, with low genetic variability as a consequence of isolation and population size reduction. Conservation management practices have been implemented, but their efficacy has not been addressed. We genotyped individuals collected 1997–2014 to determine temporal trends in population genetic variation, structure, and effective size. Observed and expected heterozygosity and allelic richness revealed temporally stable, but low, levels of genetic variation. Positive levels of inbreeding were found in each year. There was weak genetic structure among years, which can be attributed to increased effects of genetic drift and inbreeding in small populations. L. sevosus exhibited an increase in effective population size, and currently has an estimated effective size of 33.0–58.6 individuals, which is approximately half the census size. This large ratio could possibly be explained by genetic compensation. We found that management practices have been effective at maintaining and improving effective size and genetic diversity, but that additional strategies need to be implemented to enhance viability of the species.

Triploid bumblebees indicate a direct cost of inbreeding in fragmented populations

Hymenopteran species with single-locus complimentary sex-determination (sl-CSD) face an additional cost of inbreeding because of a loss of diversity at the sex-determining locus. Laboratory studies of a range of Hymenoptera have found that a small percentage of diploid males produce viable diploid sperm, and that if these males mate, then the resultant females produce triploid offspring that are sterile. Here, we use microsatellite markers to determine the frequency of triploid individuals of Bombus muscorum and B. jonellus in a model island system. Triploids were found in populations of both species. Observed triploid frequencies of up to 8% were detected, and estimated total frequencies peaked at 20% with respect to normal diploid workers. For both species, triploid frequency was negatively correlated with surrogates of population size, providing direct evidence for inbreeding in small populations. Populations limited to <∼15 km(2) of suitable habitat were particularly likely to harbour triploids. Estimated total triploid frequencies were higher in B. muscorum than in B. jonellus, perhaps due to the greater dispersal range of the latter species. Implications for the conservation of rare social hymenopterans are discussed.

Condition, innate immunity and disease mortality of inbred crows

Cooperatively breeding American crows (Corvus brachyrhynchos) suffer a severe disease-mediated survival cost from inbreeding, but the proximate mechanisms linking inbreeding to disease are unknown. Here, we examine indices of nestling body condition and innate immunocompetence in relationship to inbreeding and disease mortality. Using an estimate of microsatellite heterozygosity that predicts inbreeding in this population, we show that inbred crows were in relatively poor condition as nestlings, and that body condition index measured in the first 2-33 days after hatching, in addition to inbreeding index, predicted disease probability in the first 34 months of life. Inbred nestlings also mounted a weaker response along one axis of innate immunity: the proportion of bacteria killed in a microbiocidal assay increased as heterozygosity index increased. Relatively poor body condition and low innate immunocompetence are two mechanisms that might predispose inbred crows to ultimate disease mortality. A better understanding of condition-mediated inbreeding depression can guide efforts to minimize disease costs of inbreeding in small populations.

A Simple Method to Account for Natural Selection When Predicting Inbreeding Depression

It has been widely appreciated that natural selection opposes the progress of inbreeding in small populations, thus limiting the actual inbreeding depression for fitness traits. However, no method to account for the consequences of this process has been given so far. I give a simple and intuitive method to predict inbreeding depression, taking into account the increase in selection efficiency against recessive alleles during inbreeding. It is based on the use of a "purged inbreeding coefficient" g(t) that accounts for the reduction of the probability of the deleterious homozygotes caused by the excess d of detrimental effect for deleterious alleles in the homozygous condition over its additive expectation. It is shown that the effect of purging can be important even for relatively small populations. For between-loci variable deleterious effects, accurate predictions can be obtained using the effective homozygous deleterious excess d(e), which can be estimated experimentally and is robust against variation of the ancestral effective population size. The method can be extended to any trait and it is used to predict the evolution of the mean viability or fecundity in a conservation program with equal or random family contributions.

Minimising inbreeding in small populations by rotational mating with frozen semen

Mating plans are investigated in order to minimize inbreeding in small populations when frozen semen is available. For a single dam line it was found that specific sire rotations minimized the asymptotic level of inbreeding when semen is used repeatedly from certain generations. When semen of N foundation (G0) sires is used rotationally over generations it is shown that the inbreeding level asymptotes to 1/(2(N+1) - 2). However, if only G0 sires are used then all genes will eventually descend from the founder sires. Inbreeding can be reduced further by using sires from generation one (G1) and later as this retains genes from the founder dams in the long-term gene pool. If semen from NG0 sires and N unrelated G1 sons is used rotationally then inbreeding asymptotes to (2(N-1) + 1)/(2(2N+1) - 2). When there are more founder dams than sires, the asymptotic inbreeding can be reduced even further by using the semen of half-sib G1 sires in rotation. Optimal rotations using full-sib G1 sires or generation 2 (or later) sires will lower the asymptotic inbreeding also, but generally not by much. It was found that when unlimited frozen semen from a specified group of sires was available, the optimal mating plan was achieved by selecting each generation the sire with the least co-ancestry with the current female of the dam line.

Fixed contributions designs vs. minimization of global coancestry to control inbreeding in small populations.

Populations with small census sizes are at risk because of the loss of genetic variability and the increase of inbreeding and its harmful consequences. For situations with different numbers of males and females, several hierarchical designs have been proposed to control inbreeding through the fixation of individuals' contributions. An alternative method, based on the minimization of global coancestry, has been proposed to determine contributions as to yield of the lowest levels of inbreeding in the population. We use computer simulations to assess the relative efficiency of the different methods. The results show that minimizing the global coancestry leads to equal or lower levels of inbreeding in the short and medium term, although one of the hierarchical designs provides lower asymptotic inbreeding rates and, thus, less net inbreeding in the long term. We also investigate the performance of the alternative methods against departures from the ideal conditions, such as inbred or differentially related base individuals and random failures in the expected contributions. The method of minimization of global coancestry turns out to be more flexible and robust under these realistic situations.

Genetic variation of Saxifraga paniculata Mill. (Saxifragaceae): molecular evidence for glacial relict endemism in central Europe

Saxifraga paniculata Mill. is an amphi-atlantic species that is widely distributed in the Alps but also occurs with disjunct populations in central Europe. These isolated populations are considered to be glacial relicts. In the study presented here, we analysed the genetic variation within and between populations of Saxifraga paniculata in central Europe to test whether the molecular data give evidence for the supposed relict endemism. We used RAPD analysis and the analysis of molecular variance (AMOVA) technique to investigate 30 populations of Saxifraga paniculata from different locations in central Europe and adjacent geographical areas. In the RAPD analysis, 319 fragments could be amplified of which 91.2% were polymorphic. The percentage of polymorphic bands within populations correlated significantly with population size, indicating a higher level of inbreeding in small populations. AMOVA revealed 43.60% of the variation within populations, only 15.45% between populations within locations, and 40.95% between locations. Genetic distance between locations (ΦST) correlated significantly with the geographical distance between locations, giving evidence for geographical isolation. In an UPGMA cluster analysis, based on RAPD data, the populations were grouped together according to their location. The results exhibit a strong genetic differentiation which is obviously due to genetic drift in the isolated populations. Our study therefore gives evidence for glacial relict endemism of Saxifraga paniculata in central Europe. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 11–21.

Minimizing inbreeding by managing genetic contributions across generations.

Here we present the strategy that achieves the lowest possible rate of inbreeding (DeltaF) for a population with unequal numbers of sires and dams with random mating. This new strategy results in a DeltaF as much as 10% lower than previously achieved. A simple and efficient approach to reducing inbreeding in small populations with sexes of unequal census number is to impose a breeding structure where parental success is controlled in each generation. This approach led to the development of strategies for selecting replacements each generation that were based upon parentage, e.g., a son replacing its sire. This study extends these strategies to a multigeneration round robin scheme where genetic contributions of ancestors to descendants are managed to remove all uncertainties about breeding roles over generations; i.e., male descendants are distributed as equally as possible among dams. In doing so, the sampling variance of genetic contributions within each breeding category is eliminated and consequently DeltaF is minimized. Using the concept of long-term genetic contributions, the asymptotic DeltaF of the new strategy for random mating, M sires and d dams per sire, is phi/(12M), where phi = [1 + 2((1)/(4))(d)]. Predictions were validated using Monte Carlo simulations. The scheme was shown to achieve the lowest possible DeltaF using pedigree alone and showed that further reductions in DeltaF below that obtained from random mating arise from preferential mating of relatives and not from their avoidance.

The use of frozen semen to minimize inbreeding in small populations.

In this study, we compared the average coancestry and inbreeding levels for two genetic conservation schemes in which frozen semen from a gene bank is used to reduce the inbreeding in a live population. For a simple scheme in which only semen of generation-0 (G0) sires is used, the level of inbreeding asymptotes to 1/(2N), where N is the number of newborn sires in the base generation and rate of inbreeding goes to zero. However, when only sires of G0 are selected, all genes will eventually descend from the founder sires and all genes from the founder dams are lost. We propose an alternative scheme in which N sires from generation 1 (G1), as well as the N sires from G0, have semen conserved, and the semen of G0 and G1 sires is used for dams of odd and even generation numbers, respectively. With this scheme, the level of inbreeding asymptotes to 1/(3N) and the genes of founder dams are also conserved, because 50% of the genes of sires of G1 are derived from the founder dams. A computer simulation study shows that this is the optimum design to minimize inbreeding, even if semen from later generations is available.

Intersimple sequence repeat (ISSR) variation in Lactoris fernandeziana (Lactoridaceae), a rare endemic of the Juan Fernández Archipelago, Chile

AbstractSixteen populations and 89 individuals of Lactoris fernandeziana were examined for variation in intersimple sequence repeat (ISSR) banding patterns. The species is a rare endemic of Masatierra Island in the Juan Fernández Archipelago, and is the only member of the endemic family Lactoridaceae. Five populations showed a single genotype whereas the other 11 populations had from two to 16 multilocus genotypes. Over 73% of the ISSR diversity occurred across populations, with only about 27% within populations. Diversity among populations results from the presence of different subsets of loci within each population rather than unique loci within populations; only two populations displayed novel loci, with one and three in each. Levels of differentiation at ISSR loci among populations are not correlated with geographic distance on Masatierra; rather, the pattern of variation is mosaic. The presence of differentiated local populations is concordant with the geitonogamous breeding system of the species and suggests low levels of long distance pollen or seed dispersal. The mosaic pattern of ISSR variation on Masatierra may result, in part, from drift and inbreeding in small populations following fragmentation of a once more continuous distribution of Lactoris with the formation of canyons by erosion. Also, the generation of new ISSR loci by mutation could occur with rare, sporadic gene flow among populations accounting for the mosaic pattern of variation and the paucity of unique alleles within populations. The ISSR results for Lactoris suggest that studies of morphological, ecological and physiological features may elucidate differentiation among populations of L. fernandeziana. Field studies have demonstrated that plants occur both in the dense forest understory and in the full sunlight in forest openings.

Breeding population size of a fragmented population of a Costa Rican dry forest tree species.

Pollen immigration can offset the effects of genetic drift and inbreeding in small populations. To understand the genetic consequences of forest fragmentation, estimates of pollen flow into remnant fragments are essential. Such estimates are straightforward for plants with singly sired, multiseeded fruits, since the pollen donor genotype for each fruit can be unambiguously reconstructed through full-sib genealogical analyses. Allozyme analyses were used to estimate pollen donor numbers from the progeny of fruits of the tropical dry forest tree Enterolobium cyclocarpum in a small (9.8 ha) fragmented population (N = 11) over three reproductive seasons (1994, 1995, and 1996). These analyses indicate that each tree receives pollen from many pollen donors. When data are pooled for the site, estimated maximum pollen donor pool sizes in all years exceed the number of individuals (56) in the 227 ha study area. Although unidentified pollen donors may be located as close as 250 m to the study trees, the number of unidentified pollen donors indicates that individuals in this forest fragment are part of a large network of reproductively active individuals.

Effect of Population Outcrossing Rate on Inbreeding Depression in Pinus contorta var. murrayana Seedlings

Self and cross families from three populations (A, low-density, ecologically marginal site for lodgepole pine, and B + C, normal sites) were cultured in a common outdoor nursery for 2 yrs. Previous results had shown higher natural selfing rates and lower inbreeding depression in embryo survival in A than in B + C. In the nursery test, selfing decreased means of size traits, retarded phenological development, increased variance among families within populations, increased the coefficient of within-family variance, and increased within-family skewness. The selfing depression of mean values was moderately less and the selfing inflation of within-plot variation was much less in A than in B + C. Results were compatible with the idea that the higher selfing rate in A had purged both severely deleterious alleles affecting embryo survival and severely deleterious alleles affecting later life-cycle traits related to plant size. Purging partially mitigated the genetic consequences associated with increased inbreeding in small populations, but even with purging, population A retained a large inbreeding depression in both embryonic and seedling traits.

Leopard (Panthera pardus ciscaucasica) in Armenia: basic trends, dangers and hopes

SUMMARY This article describes ecological, genetic, psychological, juridical and economic aspects of the leopard (Panthera pardus ciscaucasica) conservation in Armenia. It also suggests certain tools for species preservation by means of ecotourism and ungulate breeding development and provides an overview of global perils to leopard, namely the cat skin trade, sport hunting and eradication by shepherds and livestock breeders. In the short-term perspective, the current abundance of leopard (25 individuals) ensures the reproduction group size (effective population size) of 15–20 animals and loss of genetic variability (heterozygosity) at a rate 2.5–3% per generation. Individual range and biomass values are 89.2 km2 and 0.5 kg/km2, respectively. If today's trends remain the same, leopard population in Armenia is likely to run down to extinction after approximately 30 generations. These data, however, do not imply the leopard's early demise as its ability to overcome the problem of inbreeding in small populations by adaptability and natural selection is still unknown. In psychological terms, the leopard has the highest preservation value of intangible characteristics — existence value, bequest value, option value and vicarious (recreational) value. The juridical and economic backgrounds of the man—leopard conflict are confined to the assessment of different views on the illegal killing of leopards by farmers and conservationists. Owners of the domestic animals attacked by leopards need full reimbursement of material detriment, while wildlife rangers and conservation authorities blame farmers for deliberate killing of the predators and punish them without understanding the reasons which instigate the livestock breeders to commit the misdeed.

Genetic Variation and Outcrossing Rate in Relation to Population Size in Gentiana pneumonanthe L

The amount of genetic variation in the rare perennial herb Gentiana pneumonanthe L. was determined to explore its relation to population size. Differences in isozyme variation between maternal plants and their offspring were used to investigate the relationship between population size and outcrossing rate. In 25 populations in The Netherlands, differing in size from 1 to more than 50,000 flowering individuals, 16 allozyme loci were analyzed on leaves of maternal plants and offspring grown in a greenhouse. Population size was significantly positively correlated with the proportion of polymorphic loci, but only marginally with heterozygosity and the mean effective number of alleles. Most of the studied populations were characterized by a complete absence of rare alleles, and F‐statistics suggest relatively high levels of genetic differentiation among populations and thus a low level of gene flow. Leaf samples (maternal) were mostly in Hardy‐Weinberg equilibrium, while several offspring samples showed an excess of homozygotes, which suggests selection favoring heterozygotes. Because most small populations consist only of adult survivors from formerly larger populations, this may partly explain the absence of a clear relationship between genetic variation of the maternal plants and population size. A significant positive correlation was found between the level of cross‐fertilization and population size. From these results, we conclude that, to some degree, small populations have a reduced level of genetic variation, while their present isolation in nature reserves has resulted in a very limited interpopulational gene flow level. At present a higher level of inbreeding in small populations contributes to a further loss of genetic variation and may also result in reduced offspring fitness.

Demographic and genetic effects on reproduction as related to population size in a rare, perennial herb, Senecio integrifolius (Asteraceae)

Seed-set of the rare and threatened plant Senecio integrifolius increased significantly with population size. Experimental studies as well as field observations showed this to be due to density-dependent seed-set (Allee effect). Hand-pollination revealed lower seed-set, and a lower germination rate of inbred progeny than of outbred progeny, with great differences among populations. Contrary to general predictions in models of minimum viable population sizes, the present study indicates little negative effects of inbreeding in small populations. A genetic load model was invoked to explain the results, hypothesizing that purging of deleterious alleles in small populations has reduced inbreeding depression. However, no clear correlation between population size and genetic load was found. The results in this paper suggest that demographic and environmental factors are of greater immediate importance than population genetics in determining extinction probabilities of small plant populations.