Analysis of founder representation in pedigrees: Founder equivalents and founder genome equivalents

The concepts of “founder equivalent” and “founder genome equivalent” are introduced to facilitate analysis of the founding stocks of captive or other populations for which pedigrees are available. The founder equivalents of a population are the number of equally contributing founders that would be expected to produce the same genetic diversity as in the population under study. Unequal genetic contributions by founders decrease the founder equivalents, portend greater inbreeding in future generations than would be necessary, and reflect a greater loss of the genetic diversity initially present in the founders. The number of founder genome equivalents of a population is that number of equally contributing founders with no random loss of founder alleles in descendants that would be expected to produce the same genetic diversity as in the population under study. The number of founder genome equivalents is approximately that number of wild-caught animals that would be needed to obtain the same amount of genetic diversity as is in the descendant captive population. Founder equivalents and founder genome equivalents allow comparison of the genetic merits of adding new wild-caught stock vs. further equalizing founder representations in a captive population.     

Change in genetic size of small-closed populations: Lessons from a domestic mammal population

The aim of this study was to monitor changes in genetic size of a small-closed population of Iranian Zandi sheep, by using pedigree information from animals born between 1991 and 2005. The genetic size was assessed by using measures based on the probability of identity-by-descend of genes (coancestry, f, and effective population size, N(e) ), as well as measures based on probability of gene origin (effective number of founders, f(e) , effective number of founder genomes, f(g) , and effective number of non-founder genomes, f(ne) ). Average coancestry, or the degree of genetic similarity of individuals, increased from 0.81% to 1.44% during the period 1993 to 2005, at the same time that N(e) decreased from 263 to 93. The observed trend for f(e) was irregular throughout the experiment in a way that f(e) was 68, 87, 77, 92, and 80 in 1993, 1996, 1999, 2002, and 2005, respectively. Simultaneously, f(g) , the most informative effective number, decreased from 61 to 35. The index of genetic diversity (GD) which was obtained from estimates of f(g) , decreased about 2% throughout the period studied. In addition, a noticeable reduction was observed in the estimates of f(ne) from 595 in 1993 to 61 in 2005. The higher than 1 ratio of f(e) to f(g) indicated the presence of bottlenecks and genetic drift in the development of this population of Zandi sheep. From 1993 to 1999, f(ne) was much higher than f(e) , thereby indicating that with respect to loss of genetic diversity, the unequal contribution of founders was more important than the random genetic drift in non-founder generations. Subsequently, random genetic drift in non-founder generations was the major reason for f(e) > f(ne) . The minimization of average coancestry in new reproductive individuals was recommended as a means of preserving the population against a further loss in genetic diversity.     

Genetic and demographic founder effects have long‐term fitness consequences for colonising populations

Colonisation is a fundamental ecological and evolutionary process that drives the distribution and abundance of organisms. The initial ability of colonists to establish is determined largely by the number of founders and their genetic background. We explore the importance of these demographic and genetic properties for longer term persistence and adaptation of populations colonising a novel habitat using experimental populations of Tribolium castaneum. We introduced individuals from three genetic backgrounds (inbred – outbred) into a novel environment at three founding sizes (2–32), and tracked populations for seven generations. Inbreeding had negative effects, whereas outbreeding generally had positive effects on establishment, population growth and long‐term persistence. Severe bottlenecks due to small founding sizes reduced genetic variation and fitness but did not prevent adaptation if the founders originated from genetically diverse populations. Thus, we find important and largely independent roles for both demographic and genetic processes in driving colonisation success.     

INCREASED PROBABILITY OF EXTINCTION DUE TO DECREASED GENETIC EFFECTIVE POPULATION SIZE: EXPERIMENTAL POPULATIONS OF CLARKIA PULCHELLA

We established replicated experimental populations of the annual plant Clarkia pulchella to evaluate the existence of a causal relationship between loss of genetic variation and population survival probability. Two treatments differing in the relatedness of the founders, and thus in the genetic effective population size (N_e), were maintained as isolated populations in a natural environment. After three generations, the low N_e treatment had significantly lower germination and survival rates than did the high N_e treatment. These lower germination and survival rates led to decreased mean fitness in the low N_e populations: estimated mean fitness in the low N_e populations was only 21% of the estimated mean fitness in the high N_e populations. This inbreeding depression led to a reduction in population survival: at the conclusion of the experiment, 75% of the high N_e populations were still extant, whereas only 31% of the low N_e populations had survived. Decreased genetic effective population size, which leads to both inbreeding and the loss of alleles by genetic drift, increased the probability of population extinction over that expected from demographic and environmental stochasticity alone. This demonstrates that the genetic effective population size can strongly affect the probability of population persistence.     

Small population size and extremely low levels of genetic diversity in island populations of the platypus, Ornithorhynchus anatinus

Genetic diversity generally underpins population resilience and persistence. Reductions in population size and absence of gene flow can lead to reductions in genetic diversity, reproductive fitness, and a limited ability to adapt to environmental change increasing the risk of extinction. Island populations are typically small and isolated, and as a result, inbreeding and reduced genetic diversity elevate their extinction risk. Two island populations of the platypus, Ornithorhynchus anatinus, exist; a naturally occurring population on King Island in Bass Strait and a recently introduced population on Kangaroo Island off the coast of South Australia. Here we assessed the genetic diversity within these two island populations and contrasted these patterns with genetic diversity estimates in areas from which the populations are likely to have been founded. On Kangaroo Island, we also modeled live capture data to determine estimates of population size. Levels of genetic diversity in King Island platypuses are perilously low, with eight of 13 microsatellite loci fixed, likely reflecting their small population size and prolonged isolation. Estimates of heterozygosity detected by microsatellites (H(E)= 0.032) are among the lowest level of genetic diversity recorded by this method in a naturally outbreeding vertebrate population. In contrast, estimates of genetic diversity on Kangaroo Island are somewhat higher. However, estimates of small population size and the limited founders combined with genetic isolation are likely to lead to further losses of genetic diversity through time for the Kangaroo Island platypus population. Implications for the future of these and similarly isolated or genetically depauperate populations are discussed.     

Inbreeding depression in insular and central populations of Peromyscus mice

We tested the hypothesis that small, isolated populations would show less depression in fitness when inbred than would large, central populations. Laboratory stocks of Peromyscus leucopus and P. polionotus were established from insular, peninsular, and central populations. The isolated populations had one-third to one-half the genic diversity of central populations. Responses to inbreeding were highly varied: some populations had smaller litters, others experienced higher mortality, some showed slower growth rates, and one displayed no measurable effects when inbred. These results suggest that inbreeding depression is controlled by a small number of genes and that the size of the genetic load depends on which alleles are present in the founders of a population. The severity of fitness depression in inbred litters did not correlate with initial genic diversity of the stocks nor, therefore, with the size of the wild populations. Fitness measures appeared linearly related to the inbreeding coefficient of the liters, with no diminution of deleterious effects through subsequent generations of inbreeding. Thus overdominance of fitness traits probably contributed as much to the genetic load as did deleterious recessive alleles. The inbreeding level of the dam negatively affected the size, growth, and survival of litters only in genetically diverse populations, indicating that the load of recessive alleles negatively impacting maternal care may have been reduced by selection in the more peripheral populations during past bottlenecks.     

Genetic Diversity and the Survival of Populations

Abstract: In this comprehensive review, a range of factors is considered that may influence the significance of genetic diversity for the survival of a population. Genetic variation is essential for the adaptability of a population in which quantitatively inherited, fitness-related traits are crucial. Therefore, the relationship between genetic diversity and fitness should be studied in order to make predictions on the importance of genetic diversity for a specific population. The level of genetic diversity found in a population highly depends on the mating system, the evolutionary history of a species and the population history (the latter is usually unknown), and on the level of environmental heterogeneity. An accurate estimation of fitness remains complex, despite the availability of a range of direct and indirect fitness parameters. There is no general relationship between genetic diversity and various fitness components. However, if a lower level of heterozygosity represents an increased level of inbreeding, a reduction in fitness can be expected. Molecular markers can be used to study adaptability or fitness, provided that they represent a quantitative trait locus (QTL) or are themselves functional genes involved in these processes. Next to a genetic response of a population to environmental change, phenotypic plasticity in a genotype can affect fitness. The relative importance of plasticity to genetic diversity depends on the species and population under study and on the environmental conditions. The possibilities for application of current knowledge on genetic diversity and population survival for the management of natural populations are discussed.     

Source population characteristics affect heterosis following genetic rescue of fragmented plant populations

Understanding the relative importance of heterosis and outbreeding depression over multiple generations is a key question in evolutionary biology and is essential for identifying appropriate genetic sources for population and ecosystem restoration. Here we use 2455 experimental crosses between 12 population pairs of the rare perennial plant Rutidosis leptorrhynchoides (Asteraceae) to investigate the multi-generational (F₁, F₂, F₃) fitness outcomes of inter-population hybridization. We detected no evidence of outbreeding depression, with inter-population hybrids and backcrosses showing either similar fitness or significant heterosis for fitness components across the three generations. Variation in heterosis among population pairs was best explained by characteristics of the foreign source or home population, and was greatest when the source population was large, with high genetic diversity and low inbreeding, and the home population was small and inbred. Our results indicate that the primary consideration for maximizing progeny fitness following population augmentation or restoration is the use of seed from large, genetically diverse populations.     

Long-term genetic monitoring reveals contrasting changes in the genetic composition of newly established populations of the intertidal snail Bembicium vittatum

Newly established populations are susceptible to founder events that reduce genetic variation. This may be counterbalanced by gene flow after populations become established or founders coming from genetically different populations. However, initial gains in genetic diversity may be short-lived if there is limited mixing between lineages and subsequent inbreeding, or if one lineage sweeps to fixation through selection or genetic drift. Here, we report on the genetic changes taking place within two newly established populations of intertidal snail over a 15-year period (～ 10 generations). Each translocation was set up using multiple, genetically distinct source populations. Our data show that higher levels of variation in the translocated populations compared to the source populations were maintained over time for both nuclear (microsatellite) and mitochondrial genes. Small changes in allele and haplotype frequencies were observed in the source populations and in one of the translocated populations, but marked changes were evident in the other, where there was a dramatic shift towards the genetic make-up of one of the source populations. These genetic changes occurred despite relatively large numbers of founders (200-374 adults) and no evidence of the population experiencing a severe reduction in effective population size. Our study shows that the genetic composition of newly established populations can vary greatly over time and that genetic outcomes can be highly variable, and significantly different from initial expectations, even when they are established using high numbers of individuals and involve source populations from the same geographic regions.     

Limited Reintroduction Does Not Always Lead to Rapid Loss of Genetic Diversity: An Example from the American Chestnut (Castanea dentata; Fagaceae)

In restoring species, reasons for introducing limited numbers of individuals at different locations include costs of introduction and maintenance, limited founder supply, and risk “bet hedging.” However, populations initiated from few founders may experience increased genetic drift, inbreeding, and diversity loss. We examined the genetic diversity of an isolated stand of more than 5,000 American chestnut trees relative to that of the 9 surviving stand founders (out of 10 total) planted in the 1880s. We used minisatellite DNA probes to reveal 84 genetic markers (circa 24 loci) among the nine founders, and their genetic diversity was compared with three separate plots of descendant trees, as well as with two natural stands. The descendants were circa 7.3% more heterozygous than the founders (mean estimated H= 0.556 vs. 0.518, respectively; p < 0.0001). Genetic differentiation was not pronounced (F_ST < 0.031), and no markers, including those at low frequency among the founders, were lost in the descendants. The founders and natural transects were not significantly different in H or similarity (mean proportion of bands shared). Special planting or mating protocols for establishment of a vigorous American chestnut population from a low number of founders may not be required to avoid strong effects of genetic drift and inbreeding. These results demonstrate that loss of genetic diversity following reintroduction of a limited number of founders is not always inevitable, such as this case where the species is highly outcrossing, expression of heterozygous advantage may occur, the original founders remain as gene contributors over generations, and the establishing population expands constantly and rapidly.     

Development of a Chinese-Indian hybrid (Chindian) rhesus macaque colony at the California National Primate Research Center by introgression

Background  Fullbred Chinese and Indian rhesus macaques represent genetically distinct populations. The California National Primate Research Center introduced Chinese founders into its Indian-derived rhesus colony in response to the 1978 Indian embargo on exportation of animals for research and the concern that loss of genetic variation in the closed colony would hamper research efforts. The resulting hybrid rhesus now number well over a thousand animals and represent a growing proportion of the animals in the colony.
Methods  We characterized the population genetic structure of the hybrid colony and compared it with that of their pure Indian and Chinese progenitors.
Results  The hybrid population contains higher genetic diversity and linkage disequilibrium than their full Indian progenitors and represents a resource with unique research applications.
Conclusions  The genetic diversity of the hybrids indicates that the strategy to introduce novel genes into the colony by hybridizing Chinese founders and their hybrid offspring with Indian-derived animals was successful.     

Newly evolved genes: Moving from comparative genomics to functional studies in model systems

Genes are gained and lost over the course of evolution. A recent study found that over 1,800 new genes have appeared during primate evolution and that an unexpectedly high proportion of these genes are expressed in the human brain. But what are the molecular functions of newly evolved genes and what is their impact on an organism's fitness? The acquisition of new genes may provide a rich source of genetic diversity that fuels evolutionary innovation. Although gene manipulation experiments are not feasible in humans, studies in model organisms, such as Drosophila melanogaster, have shown that new genes can quickly become integrated into genetic networks and become essential for survival or fertility. Future studies of new genes, especially chimeric genes, and their functions will help determine the role of genetic novelty in the adaptation and diversification of species.     

Genetic structure and individual performance following a recent founding event in a small lizard

Reintroduced populations of threatened species are often founded by a small number of individuals, but maximising genetic diversity is often a criterion for founder selection. Reintroduction of pregnant females has been proposed as a means of maximising productivity and genetic diversity, but it is unclear whether the release of pregnant females increases the effective number of founders. Ten male and 20 gravid female egg-laying skinks (Oligosoma suteri) were reintroduced to Korapuki Island from Green Island, New Zealand in 1992. We sampled the populations on both Green and Korapuki Islands to examine the effect of reintroduction on the genetic structure and fitness of egg-laying skinks following release. The population on Korapuki Island showed multiple genetic signatures of a bottleneck that were not detected in the population on Green Island. At the individual level, juveniles on Korapuki Island were more homozygous than adults on Korapuki and Green Islands. However, we did not find evidence of inbreeding depression using two performance-based surrogates of fitness. Further, the population on Korapuki Island had a significantly larger effective population size than would have been expected by reintroduction of 30 skinks, based on 10,000 simulated populations. The reintroduction of gravid females aided in increasing the effective number of founders, and may be a viable option for maximizing genetic diversity in reintroduced populations, particularly for long-lived species. However, the continued loss of genetic variation in reintroduced populations may have more insidious long-term consequences, such as the loss of adaptive potential, which cannot be assessed in the short-term.     

Minimizing kinship in captive breeding programs

Captive populations of endangered species are managed to preserve genetic diversity and retain reproductive fitness. Minimizing kinship (MK) has been predicted to maximize the retention of gene diversity in pedigreed populations with unequal founder representation. MK was compared with maximum avoidance of inbreeding (MAI) and random choice of parents (RAND) using Drosophila melanogaster. Forty replicate populations of each treatment were initiated with unequal founder representation and managed for four generations. MK retained significantly more gene diversity and allelic diversity based on six microsatellite loci and seven allozyme loci than MAI or RAND. Reproductive fitness under both benign and competitive conditions did not differ significantly among treatments. Of the methods considered, MK is currently the best available for the genetic management of captive populations. Zoo Biol 16:377–389, 1997. © 1997 Wiley-Liss, Inc.     

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.     

The evolution of genetic canalization under fluctuating selection

Abstract.— If the direction of selection changes from generation to generation, the ability to respond to selection is maladaptive: the response to selection in one generation leads to reduced fitness in the next. Because the response is determined by the amount of genetic variance expressed at the phenotypic level, rapidly fluctuating selection should favor modifier genes that reduce the phenotypic effect of alleles segregating at structural loci underlying the trait. Such reduction in phenotypic expression of genetic variation has been named "genetic canalization." I support this argument with a series of two- and multilocus models with alternating linear selection and Gaussian selection with fluctuating optimum. A canalizing modifier gene affects the fitness of its carriers in three ways: (1) it reduces the phenotypic consequences of genetic response to previous selection; (2) it reduces the genetic response to selection, which is manifested as linkage disequilibrium between the modifier and structural loci; and (3) it reduces the phenotypic variance. The first two effects reduce fitness under directional selection sustained for several generations, but improve fitness when the direction of selection has just been reversed. The net effect tends to favor a canalizing modifier under rapidly fluctuating selection regimes (period of eight generations or less). The third effect improves fitness of the modifier allele if the fitness function is convex and reduces it if the function is concave. Under fluctuating Gaussian selection, the population is more likely to experience the concave portion of the fitness function when selection is stronger. Therefore, only weak to moderately strong fluctuating Gaussian selection favors genetic canalization. This paper considerably broadens the conditions that favor genetic canalization, which so far has only been postulated to evolve under long-term stabilizing selection.     

Genetic assessment of the Iberian wolf Canis lupus signatus captive breeding program

The main goal of ex situ conservation programs is to improve the chances of long term survival of natural populations by founding and managing captive colonies that can serve as a source of individuals for future reintroductions or to reinforce existing populations. The degree in which a captive breeding program has captured the genetic diversity existing in the source wild population has seldom been evaluated. In this study we evaluate the genetic diversity in wild and captive populations of the Iberian wolf, Canis lupus signatus, in order to assess how much genetic diversity is being preserved in the ongoing ex situ conservation program for this subspecies. A sample of domestic dogs was also included in the analysis for comparison. Seventy-four wolves and 135 dogs were genotyped at 13 unlinked microsatellite loci. The results show that genetic diversity in Iberian wolves is comparable in magnitude to that of other wild populations of gray wolf. Both the wild and the captive Iberian wolf populations have a similarly high genetic diversity indicating that no substantial loss of diversity has occurred in the captive-breeding program. The effective number of founders of the program was estimated as ∼ ∼16, suggesting that all founders in the studbook pedigree were genetically independent. Our results emphasize also the genetic divergence between wolves and domestic dogs and indicate that our set of 13 microsatellite loci provide a powerful diagnostic test to distinguish wolves, dogs and their hybrids.     

Population demography and heterozygosity–fitness correlations in natural guppy populations: An examination using sexually selected fitness traits

Heterozygosity–fitness correlations (HFCs) have been examined in a wide diversity of contexts, and the results are often used to infer the role of inbreeding in natural populations. Although population demography, reflected in population‐level genetic parameters such as allelic diversity or identity disequilibrium, is expected to play a role in the emergence and detectability of HFCs, direct comparisons of variation in HFCs across many populations of the same species, with different genetic histories, are rare. Here, we examined the relationship between individual microsatellite heterozygosity and a range of sexually selected traits in 660 male guppies from 22 natural populations in Trinidad. Similar to previous studies, observed HFCs were weak overall. However, variation in HFCs among populations was high for some traits (although these variances were not statistically different from zero). Population‐level genetic parameters, specifically genetic diversity levels (number of alleles, observed/expected heterozygosity) and measures of identity disequilibrium (g2 and heterozygosity–heterozygosity correlations), were not associated with variation in population‐level HFCs. This latter result indicates that these metrics do not necessarily provide a reliable predictor of HFC effect sizes across populations. Importantly, diversity and identity disequilibrium statistics were not correlated, providing empirical evidence that these metrics capture different essential characteristics of populations. A complex genetic architecture likely underpins multiple fitness traits, including those associated with male fitness, which may have reduced our ability to detect HFCs in guppy populations. Further advances in this field would benefit from additional research to determine the demographic contexts in which HFCs are most likely to occur.     

Effects of a recent founding event and intrinsic population dynamics on genetic diversity in an ungulate population

Maintenance of genetic diversity has recently become a management goal for a number of species, due to its importance for present and future population viability. Genetic drift, primarily through differential reproductive success and inbreeding, can accelerate the loss of genetic diversity in recently recovered populations. We attempt to quantify the consequences of these factors on the genetic diversity contained in a small, recently founded wood bison (Bison bison athabascae) population by examining the genetic variation in this conservation herd, the calves born therein, and its large source population. The Hook Lake Wood Bison Recovery Project was initiated to found a disease-free herd of wood bison containing a representative amount of the genetic diversity present in the Wood Buffalo National Park metapopulation. Levels of diversity in the Hook Lake Wood Bison Recovery Project founders are higher than in previous salvage attempts. To examine the effects of differential reproductive success on this population, we monitored parentage of the calves born in the Hook Lake Wood Bison Recovery Project for 3 years since the founders reached sexual maturity. Two of the male founders sired over 90% of the offspring born in this population, which has led to a reduction in diversity in their calves. Monitoring of reproductive success, and incorporation of selective breeding strategies will be required to reduce the rate at which genetic diversity is lost from this small, isolated population. These steps should occur in other recovery projects, particularly when a small number of individuals are capable of dominating reproduction.     

The impact of translocations on neutral and functional genetic diversity within and among populations of the Seychelles warbler

Translocations are an increasingly common tool in conservation. The maintenance of genetic diversity through translocation is critical for both the short‐ and long‐term persistence of populations and species. However, the relative spatio‐temporal impacts of translocations on neutral and functional genetic diversity, and how this affects genetic structure among the conserved populations overall, have received little investigation. We compared the impact of translocating different numbers of founders on both microsatellite and major histocompatibility complex (MHC) class I diversity over a 23‐year period in the Seychelles warbler (Acrocephalus sechellensis). We found low and stable microsatellite and MHC diversity in the source population and evidence for only a limited loss of either type of diversity in the four new populations. However, we found evidence of significant, but low to moderate, genetic differentiation between populations, with those populations established with fewer founders clustering separately. Stochastic genetic capture (as opposed to subsequent drift) was the main determinant of translocated population diversity. Furthermore, a strong correlation between microsatellite and MHC differentiation suggested that neutral processes outweighed selection in shaping MHC diversity in the new populations. These data provide important insights into how to optimize the use of translocation as a conservation tool.