Heterozygosity is unrelated to adult fitness measures in a large, noninbred population of great tits (Parus major)

The extent to which heterozygosity-fitness correlations (HFCs) are expected in wild populations is an important and unresolved question in evolutionary biology, because it relates to our understanding of the genetic architecture of fitness. Here, we report a study of HFCs in a wild, noninbred population of great tits (Parus major), based on a sample comprising 281 individuals typed at 26 markers, resulting in a data set comprising over 5600 genotypes. We regressed pedigree-derived f-score and multilocus genetic diversity against eight life-history traits known to be associated with fitness in this population, including lifetime reproductive success (LRS), as well as several morphological traits under weak selection. We found no evidence for either multilocus or single-locus HFCs for any morphological or fitness trait, and further found no evidence that effect sizes were stronger for those life-history traits more closely associated with reproductive fitness. This result may, in part, be explained by the fact that we found no evidence that our set of 26 markers had any power to infer genome-wide heterozygosity in this population and that marker-derived heterozygosity was uncorrelated with pedigree-derived f-score. Overall, these results emphasize the fact that the often-reported strong HFCs detected in small, inbred populations do not reflect a general phenomenon of increasing individual reproductive fitness with increasing heterozygosity.     

Heterozygosity–fitness correlations and their relevance to studies on inbreeding depression in threatened species

The majority of reported multilocus heterozygosity–fitness correlations (HFCs) are from large, outbred populations, and their relevance to studies on inbreeding depression in threatened populations is often stressed. The results of such HFC studies conducted on outbred populations may be of limited application to threatened population management, however, as bottlenecked populations exhibit increased incidence of inbreeding, increased linkage disequilibrium, reduced genetic diversity and possible effects of historical inbreeding such as purging. These differences may affect both our ability to detect inbreeding depression in threatened species, and our interpretation of the underlying mechanisms for observed heterozygosity–fitness relationships. The study of HFCs in outbred populations is of interest in itself, but the results may not translate directly to threatened populations that have undergone severe bottlenecks.     

Assessment of identity disequilibrium and its relation to empirical heterozygosity fitness correlations: a meta‐analysis

Heterozygosity fitness correlations (HFCs) have frequently been used to detect inbreeding depression, under the assumption that genome‐wide heterozygosity is a good proxy for inbreeding. However, meta‐analyses of the association between fitness measures and individual heterozygosity have shown that often either no correlations are observed or the effect sizes are small. One of the reasons for this may be the absence of variance in inbreeding, a requisite for generating general‐effect HFCs. Recent work has highlighted identity disequilibrium (ID) as a measure that may capture variance in the level of inbreeding within a population; however, no thorough assessment of ID in natural populations has been conducted. In this meta‐analysis, we assess the magnitude of ID (as measured by the g₂ statistic) from 50 previously published HFC studies and its relationship to the observed effect sizes of those studies. We then assess how much power the studies had to detect general‐effect HFCs, and the number of markers that would have been needed to generate a high expected correlation (r² = 0.9) between observed heterozygosity and inbreeding. Across the majority of studies, g₂ values were not significantly different than zero. Despite this, we found that the magnitude of g₂ was associated with the average effect sizes observed in a population, even when point estimates were nonsignificant. These low values of g₂ translated into low expected correlations between heterozygosity and inbreeding and suggest that many more markers than typically used are needed to robustly detect HFCs.     

Heterozygosity–fitness correlations in a declining seabird population

Loss of genetic diversity is thought to lead to increased risk of extinction in endangered populations due to decreasing fitness of homozygous individuals. Here, we evaluated the presence of inbreeding depression in a long‐lived seabird, the European shag (Phalacrocorax aristotelis), after a severe decline in population size by nearly 70%. During three reproductive seasons, 85 breeders were captured and genotyped at seven microsatellite loci. Nest sites were monitored during the breeding season to estimate reproductive success as the number of chicks surviving to full‐size‐grown per nest. Captured birds were tagged with a ring with an individual code, and resighting data were collected during 7‐year period. We found a strong effect of multilocus heterozygosity on female reproductive performance, and a significant, although weaker, effect on breeder survival. However, our matrix population model suggests that this relatively small effect of genetic diversity on breeder survival may have a profound effect on fitness. This highlights the importance of integrating life history consequences in HFC studies. Importantly, heterozygosity was correlated across loci, suggesting that genomewide effects, rather than single loci, are responsible for the observed HFCs. Overall, the HFCs are a worrying symptom of genetic erosion in this declining population. Many long‐lived species are prone to extinction, and future studies should evaluate the magnitude of fitness impact of genetic deterioration on key population parameters, such as survival of breeders.     

Using heterozygosity–fitness correlations to study inbreeding depression in an isolated population of white‐tailed deer founded by few individuals

A heterozygosity–fitness correlations (HFCs) may reflect inbreeding depression, but the extent to which they do so is debated. HFCs are particularly likely to occur after demographic disturbances such as population bottleneck or admixture. We here study HFC in an introduced and isolated ungulate population of white‐tailed deer Odocoileus virginianus in Finland founded in 1934 by four individuals. A total of 422 ≥ 1‐year‐old white‐tailed deer were collected in the 2012 hunting season in southern Finland and genotyped for 14 microsatellite loci. We find significant identity disequilibrium as estimated by g₂. Heterozygosity was positively associated with size‐ and age‐corrected body mass, but not with jaw size or (in males) antler score. Because of the relatively high identity disequilibrium, heterozygosity of the marker panel explained 51% of variation in inbreeding. Inbreeding explained approximately 4% of the variation in body mass and is thus a minor, although significant source of variation in body mass in this population. The study of HFC is attractive for game‐ and conservation‐oriented wildlife management because it presents an affordable and readily used approach for genetic monitoring that allowing identification of fitness costs associated with genetic substructuring in what may seem like a homogeneous population.     

On the correlation between heterozygosity and fitness in natural populations

Three primary hypotheses currently prevail for correlations between heterozygosity at a set of molecular markers and fitness in natural populations. First, multilocus heterozygosity-fitness correlations might result from selection acting directly on the scored loci, such as at particular allozyme loci. Second, significant levels of linkage disequilibrium, as in recently bottlenecked-and-expanded populations, might cause associations between the markers and fitness loci in the local chromosomal vicinity. Third, in partially inbred populations, heterozygosity at the markers might reflect variation in the inbreeding coefficient and might associate with fitness as a result of effects of homozygosity at genome-wide distributed loci. Despite years of research, the relative importance of these hypotheses remains unclear. The screening of heterozygosity at polymorphic DNA markers offers an opportunity to resolve this issue, and relevant empirical studies have now emerged. We provide an account of the recent progress on the subject, and give suggestions on how to distinguish between the three hypotheses in future studies.     

Heterozygosity-fitness correlations among wild populations of European tree frog (Hyla arborea) detect fixation load

Quantifying the impacts of inbreeding and genetic drift on fitness traits in fragmented populations is becoming a major goal in conservation biology. Such impacts occur at different levels and involve different sets of loci. Genetic drift randomly fixes slightly deleterious alleles leading to different fixation load among populations. By contrast, inbreeding depression arises from highly deleterious alleles in segregation within a population and creates variation among individuals. A popular approach is to measure correlations between molecular variation and phenotypic performances. This approach has been mainly used at the individual level to detect inbreeding depression within populations and sometimes at the population level but without consideration about the genetic processes measured. For the first time, we used in this study a molecular approach considering both the interpopulation and intrapopulation level to discriminate the relative importance of inbreeding depression vs. fixation load in isolated and non-fragmented populations of European tree frog (Hyla arborea), complemented with interpopulational crosses. We demonstrated that the positive correlations observed between genetic heterozygosity and larval performances on merged data were mainly caused by co-variations in genetic diversity and fixation load among populations rather than by inbreeding depression and segregating deleterious alleles within populations. Such a method is highly relevant in a conservation perspective because, depending on how populations lose fitness (inbreeding vs. fixation load), specific management actions may be designed to improve the persistence of populations.     

Age‐dependent,negative heterozygosity–fitness correlations and local effects in an endangered Caribbean reptile,Iguana delicatissima

Inbreeding depression can have alarming impacts on threatened species with small population sizes. Assessing inbreeding has therefore become an important focus of conservation research. In this study, heterozygosity–fitness correlations (HFCs) were measured by genotyping 7 loci in 83 adult and 184 hatchling Lesser Antillean Iguanas, Iguana delicatissima, at a communal nesting site in Dominica to assess the role of inbreeding depression on hatchling fitness and recruitment to the adult population in this endangered species. We found insignificant correlations between multilocus heterozygosity and multiple fitness proxies in hatchlings and adults. Further, multilocus heterozygosity did not differ significantly between hatchlings and adults, which suggests that the survivorship of homozygous hatchlings does not differ markedly from that of their heterozygous counterparts. However, genotypes at two individual loci were correlated with hatching date, a finding consistent with the linkage between specific marker loci and segregating deleterious recessive alleles. These results provide only modest evidence that inbreeding depression influences the population dynamics of I. delicatissima on Dominica.     

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.     

Cell‐mediated immunity and multi‐locus heterozygosity in bluethroat nestlings

Recent evidence suggests that marker‐based heterozygosity‐fitness correlations may be driven by only one or a few markers, indicating local heterozygosity effects caused by linkage disequilibrium with functional genes. In this study, we investigated the relationship between microsatellite heterozygosity and a measure of cell‐mediated immunity (phytohaemagglutinin; PHA) in bluethroat (Luscinia s. svecica) nestlings using a full‐sibling design. We found significant positive associations between PHA response and two different indices of microsatellite heterozygosity, i.e. multi‐locus heterozygosity and mean d². However, model comparisons disclosed that both associations were more likely caused by local effects rather than general effects and that the two local effects appeared to be realized through two different genetic mechanisms. Our results indicate that both the random assortment of parental chromosomes during meiosis as well as inbreeding can drive heterozygosity‐fitness correlations.     

Prediction of offspring fitness based on parental genetic diversity in endangered salmonid populations

By simulating all possible offspring genotypic combinations based on pair-wise matings in three vulnerable or endangered populations of salmonids (two Atlantic salmon Salmo salar and one Arctic charr Salvelinus alpinus ), family level estimates of potential offspring genetic diversity were calculated using several commonly used genetic diversity estimators (     ,     and H _EST). By using this approach, the genetic variability of offspring could be predicted accurately based solely on parental genotype data. In addition, significant associations between offspring genetic variability and fitness-related traits were observed in the two Atlantic salmon populations and these associations were consistent between fitness measures and either estimated or observed genetic diversity. This indicates that associations with offspring fitness measures can be predicted without genetic analysis of the offspring themselves.     

A comparison of pedigree‐ and DNA‐based measures for identifying inbreeding depression in the critically endangered Attwater's Prairie‐chicken

The primary goal of captive breeding programmes for endangered species is to prevent extinction, a component of which includes the preservation of genetic diversity and avoidance of inbreeding. This is typically accomplished by minimizing mean kinship in the population, thereby maintaining equal representation of the genetic founders used to initiate the captive population. If errors in the pedigree do exist, such an approach becomes less effective for minimizing inbreeding depression. In this study, both pedigree‐ and DNA‐based methods were used to assess whether inbreeding depression existed in the captive population of the critically endangered Attwater's Prairie‐chicken (Tympanuchus cupido attwateri), a subspecies of prairie grouse that has experienced a significant decline in abundance and concurrent reduction in neutral genetic diversity. When examining the captive population for signs of inbreeding, variation in pedigree‐based inbreeding coefficients (f_pedigree) was less than that obtained from DNA‐based methods (f_DNA). Mortality of chicks and adults in captivity were also positively correlated with parental relatedness (r_DNA) and f_DNA, respectively, while no correlation was observed with pedigree‐based measures when controlling for additional variables such as age, breeding facility, gender and captive/release status. Further, individual homozygosity by loci (HL) and parental r_DNA values were positively correlated with adult mortality in captivity and the occurrence of a lethal congenital defect in chicks, respectively, suggesting that inbreeding may be a contributing factor increasing the frequency of this condition among Attwater's Prairie‐chickens. This study highlights the importance of using DNA‐based methods to better inform management decisions when pedigrees are incomplete or errors may exist due to uncertainty in pairings.     

Inbreeding coefficient and heterozygosity–fitness correlations in unhatched and hatched song sparrow nestmates

Heterozygosity–fitness correlations use molecular measures of heterozygosity as proxy estimates of individual inbreeding coefficients (f) to examine relationships between inbreeding and fitness traits. Heterozygosity–fitness correlations partly depend on the assumption that individual heterozygosity and f are strongly and negatively correlated. Although theory predicts that this relationship will be strongest when mean f and variance in f are high, few studies of heterozygosity–fitness correlations include estimates of f based on pedigrees, which allow for more thorough examinations of the relationship between f, heterozygosity and fitness in nature. We examined relationships between pedigree‐based estimates of f, multilocus heterozygosity (MLH) and the probability of survival to hatch in song sparrow nestmates. f and MLH were weakly, but significantly negatively correlated. Inbreeding coefficient predicted the probability of survival to hatch. In contrast, MLH did not predict the probability of survival to hatch nor did it account for residual variation in survival to hatch after statistically controlling for the effects of f. These results are consistent with the expectation that heterozygosity–f correlations will be weak when mean and variance in f are low. Our results also provide empirical support for recent simulation studies, which show that variation in MLH among siblings with equal f can be large and may obscure MLH–fitness relationships.     

Genetic variability in the European bison (Bison bonasus) population from Białowieża forest over 50 years

The aim of this study was to assess potential post-bottleneck temporal genetic differentiation following the reintroduction of the species into the Białowieża Forest. Variability of 12 polymorphic microsatellite markers was analysed for 178 individuals born between 1955 and 2005, divided by birth year into five temporal groups. Low overall allelic richness (AR) per locus (AR = 2.0) and a low overall expected heterozygosity (H_E = 0.28) were observed. The overall F _IS was not significantly different from zero. The mean F _IS values were, however, significantly different from zero for individuals born between 1955 and 1965 ( F _IS = 0.19). A Bayesian computation was used to estimate effective population size (N_e) for each temporal group. We observed relatively small values of N_e ranging from 7.9 to 28.4. The low N_e values confirm that, despite a rapid growth of the bison population following the founder event, N_e increased only slowly.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 801–809.     

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.     

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.     

Fluctuating asymmetry and fitness correlations in two Engraulis encrasicolus populations

Correlations among several measures of fluctuating asymmetry (FA) and fitness‐related variables were assessed in two populations of the European anchovy Engraulis encrasicolus with fast growth (Aegean Sea) and slow growth (Ionian Sea), respectively. FA levels were borderline significantly higher in the Ionian than in the Aegean for some variables. Variation in otolith shape (deviation from population norm) was lower in the Ionian than the Aegean, contrary to expectation. Within the Aegean, there was no relation between any of the FA indexes and fitness estimators, while in the Ionian a composite otolith FA index was significantly negatively correlated to standard length at age only in 2 year‐old individuals. This difference between the Aegean and Ionian may have been related to the lower growth rate in the Ionian, as FA–fitness relations may be more apparent in less‐beneficial environments. The absence of significant correlations in the Aegean and the low correlation in one age group in the Ionian suggests that FA is not a sensitive indicator of individual fitness in adult E. encrasicolus.     

Assessing the genetic diversity in small farm animal populations

Genetic variation is vital for the populations to adapt to varying environments and to respond to artificial selection; therefore, any conservation and development scheme should start from assessing the state of variation in the population. There are several marker-based and pedigree-based parameters to describe genetic variation. The most suitable ones are rate of inbreeding and effective population size, because they are not dependent on the amount of pedigree records. The acceptable level for effective population size can be considered from different angles leading to a conclusion that it should be at least 50 to 100. The estimates for the effective population size can be computed from the genealogical records or from demographic and marker information when pedigree data are not available. Marker information could also be used for paternity analysis and for estimation of coancestries. The sufficient accuracy in marker-based parameters would require typing thousands of markers. Across breeds, diversity is an important source of variation to rescue problematic populations and to introgress new variants. Consideration of adaptive variation brings new aspects to the estimation of the variation between populations.     

Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria

Abstract Considerable effort has been invested in studying the relationship between fitness and genetic variability. While evidence exists both for and against positive genetic variability-fitness correlations (GFC), the possible environment and population-dependency of GFCs has seldom been tested. We investigated GFCs in common frog (Rana temporaria) tadpoles reared under different temperatures and feeding regimes in four replicate populations. Genetic variability in eight microsatellite loci in 238 parents was used to estimate heterozygosity (H) and mean expected d2 in 158-sibships (4515 offspring). Generalized linear mixed model analyses of offspring fitness traits (survival to metamorphosis, developmental and growth rate) revealed that offspring survival probability was positively correlated with H, and that relationships were similar in all four populations tested. However, significant interaction between other genetic variability measures (d2, relatedness) and treatment conditions indicated that GFCs were detectable in some, but not in all environments. Interestingly, GFCs between survival and both heterozygosity and relatedness were most pronounced in stressful environments (i.e. limited food). Developmental and growth rates were significantly associated with d2 but less with H and relatedness. Furthermore, many of these GFCs were population-specific. These results suggest--in line with the contention that expression of inbreeding depression can be environment dependent--that GFCs can also be highly sensitive to the environmental conditions under which they are measured. The results further suggest that the observed positive correlation between H and survival probability is likely to be explainable by the 'general', rather than by the 'local' or 'direct' effect hypotheses.     

Local heterozygosity-fitness correlations with global positive effects on fitness in threespine stickleback

The complex interactions between genetic diversity and evolution have important implications in many biological areas including conservation, speciation, and mate choice. A common way to study these interactions is to look at heterozygosity-fitness correlations (HFCs). Until recently, HFCs based on noncoding markers were believed to result primarily from global inbreeding effects. However, accumulating theoretical and empirical evidence shows that HFCs may often result from genes being linked to the markers used (local effect). Moreover, local effect HFCs could differ from global inbreeding effects in their direction and occurrence. Consequently, the investigation of the structure and consequences of local HFCs is emerging as a new important goal in evolutionary biology. In this study of a wild threespine stickleback (Gasterosteus aculeatus) population, we first tested the presence of significant positive or negative local effects of heterozygosity at 30 microsatellites loci on five fitness components: survival, mating success, territoriality, length, and body condition. Then, we evaluated the direction and shape of total impact of local HFCs, and estimated the magnitude of the impacts on fitness using regression coefficients and selection differentials. We found that multilocus heterozygosity was not a reliable estimator of individual inbreeding coefficient, which supported the relevance of single-locus based analyses. Highly significant and temporally stable local HFCs were observed. These were mainly positive, but negative effects of heterozygosity were also found. Strong and opposite effects of heterozygosity are probably present in many populations, but may be blurred in HFC analyses looking for global effects only. In this population, both negative and positive HFCs are apparently driving mate preference by females, which is likely to contribute to the maintenance of both additive and nonadditive genetic variance.