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.     

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.     

INBREEDING INFLUENCES WITHIN‐BROOD HETEROZYGOSITY‐FITNESS CORRELATIONS (HFCS) IN AN ISOLATED PASSERINE POPULATION

Molecular estimates of inbreeding may be made using genetic markers such as microsatellites, however the interpretation of resulting heterozygosity‐fitness correlations (HFCs) with respect to inbreeding depression is not straightforward. We investigated the relationship between pedigree‐determined inbreeding coefficients (f) and HFCs in a closely monitored, reintroduced population of Stewart Island robins (Petroica australis rakiura) on Ulva Island, New Zealand. Using a full sibling design, we focused on differences in juvenile survival associated specifically with individual sibling variation in standardized multilocus heterozygosity (SH) when expected f was identical. We found that within broods, siblings with higher SH at microsatellite loci experienced a higher probability of juvenile survival. This effect, however, was detected primarily within broods that experienced inbreeding or when inbreeding had occurred in their pedigree histories (i.e., at the parents’ level). Thus we show, for the first time in a wild population, that the strength of an HFC is partially dependent on the presence of inbreeding events in the recent pedigree history. Our results illustrate the importance of realized effects of inbreeding on genetic variation and fitness and the value of full‐sibling designs for the study of HFCs in the context of small, inbred populations.     

Evaluating the role of inbreeding depression in heterozygosity‐fitness correlations: how useful are tests for identity disequilibrium?

Heterozygosity‐fitness correlations (HFCs) have been observed for several decades, but their causes are often elusive. Tests for identity disequilibrium (ID, correlated heterozygosity between loci) are commonly used to determine if inbreeding depression is a possible cause of HFCs. We used computer simulations to determine how often ID is detected when HFCs are caused by inbreeding depression. We also used ID in conjunction with HFCs to estimate the proportion of variation (r²) in fitness explained by the individual inbreeding coefficient (F). ID was not detected in a large proportion of populations with statistically significant HFCs (sample size = 120 individuals) unless the variance of F was high (σ²(F) ≥ 0.005) or many loci were used (100 microsatellites or 1000 SNPs). For example, with 25 microsatellites, ID was not detected in 49% of populations when HFCs were caused by six lethal equivalents and σ²(F) was typical of vertebrate populations (σ²(F) ≈ 0.002). Estimates of r² between survival and F based on ID and HFCs were imprecise unless ID was strong and highly statistically significant (P ≈ 0.01). These results suggest that failing to detect ID in HFC studies should not be taken as evidence that inbreeding depression is absent. The number of markers necessary to simultaneously detect HFC and ID depends strongly on σ²(F). Thus the mating system and demography of populations, which influence σ²(F), should be considered when designing HFC studies. ID should be used in conjunction with HFCs to estimate the correlation between fitness and F, because HFCs alone reveal little about the strength of inbreeding depression.     

HETEROZYGOSITY‐FITNESS CORRELATIONS: A TIME FOR REAPPRAISAL

Owing to the remarkable progress of molecular techniques, heterozygosity‐fitness correlations (HFCs) have become a popular tool to study the impact of inbreeding in natural populations. However, their underlying mechanisms are often hotly debated. Here we argue that these “debates” rely on verbal arguments with no basis in existing theory and inappropriate statistical testing, and that it is time to reconcile HFC with its historical and theoretical fundaments. We show that available data are quantitatively and qualitatively consistent with inbreeding‐based theory. HFC can be used to estimate the impact of inbreeding in populations, although such estimates are bound to be imprecise, especially when inbreeding is weak. Contrary to common belief, linkage disequilibrium is not an alternative to inbreeding, but rather comes with some forms of inbreeding, and is not restricted to closely linked loci. Finally, the contribution of local chromosomal effects to HFC, while predicted by inbreeding theory, is expected to be small, and has rarely if ever proven statistically significant using adequate tests. We provide guidelines to safely interpret and quantify HFCs, and present how HFCs can be used to quantify inbreeding load and unravel the structure of natural populations.     

TESTING THE INFLUENCE OF FAMILY STRUCTURE AND OUTBREEDING DEPRESSION ON HETEROZYGOSITY‐FITNESS CORRELATIONS IN SMALL POPULATIONS

Theory predicts that positive heterozygosity‐fitness correlations (HFCs) arise as a consequence of inbreeding, which is often assumed to have a strong impact in small, fragmented populations. Yet according to empirical data, HFC in such populations seem highly variable and unpredictable. We here discuss two overlooked phenomena that may contribute to this variation. First, in a small population, each generation may consist of a few families. This generates random correlations between particular alleles and fitness (AFCs, allele‐fitness correlations) and results in too liberal tests for HFC. Second, in some contexts, small populations receiving immigrants may be more impacted by outbreeding depression than by inbreeding depression, resulting in negative rather than positive HFC. We investigated these processes through a case study in tadpole cohorts of Pelodytes punctatus living in small ponds. We provide evidence for a strong family structure and significant AFC in this system, as well as an example of negative HFC. By simulations, we show that this negative HFC cannot be a spurious effect of family structure, and therefore reflects outbreeding depression in the studied population. Our example suggests that a detailed examination of AFC and HFC patterns can provide valuable insights into the internal genetic structure and sources of fitness variation in small populations.     

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.     

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.     

Heterozygosity–fitness correlations in a wild mammal population: accounting for parental and environmental effects

HFCs (heterozygosity–fitness correlations) measure the direct relationship between an individual's genetic diversity and fitness. The effects of parental heterozygosity and the environment on HFCs are currently under‐researched. We investigated these in a high‐density U.K. population of European badgers (Meles meles), using a multimodel capture–mark–recapture framework and 35 microsatellite loci. We detected interannual variation in first‐year, but not adult, survival probability. Adult females had higher annual survival probabilities than adult males. Cubs with more heterozygous fathers had higher first‐year survival, but only in wetter summers; there was no relationship with individual or maternal heterozygosity. Moist soil conditions enhance badger food supply (earthworms), improving survival. In dryer years, higher indiscriminate mortality rates appear to mask differential heterozygosity‐related survival effects. This paternal interaction was significant in the most supported model; however, the model‐averaged estimate had a relative importance of 0.50 and overlapped zero slightly. First‐year survival probabilities were not correlated with the inbreeding coefficient (f); however, small sample sizes limited the power to detect inbreeding depression. Correlations between individual heterozygosity and inbreeding were weak, in line with published meta‐analyses showing that HFCs tend to be weak. We found support for general rather than local heterozygosity effects on first‐year survival probability, and g2 indicated that our markers had power to detect inbreeding. We emphasize the importance of assessing how environmental stressors can influence the magnitude and direction of HFCs and of considering how parental genetic diversity can affect fitness‐related traits, which could play an important role in the evolution of mate choice.     

Heterozygosity at a single locus explains a large proportion of variation in two fitness‐related traits in great tits: a general or a local effect?

In natural populations, mating between relatives can have important fitness consequences due to the negative effects of reduced heterozygosity. Parental level of inbreeding or heterozygosity has been also found to influence the performance of offspring, via direct and indirect parental effects that are independent of the progeny own level of genetic diversity. In this study, we first analysed the effects of parental heterozygosity and relatedness (i.e. an estimate of offspring genetic diversity) on four traits related to offspring viability in great tits (Parus major) using 15 microsatellite markers. Second, we tested whether significant heterozygosity–fitness correlations (HFCs) were due to ‘local’ (i.e. linkage to genes influencing fitness) and/or ‘general’ (genome‐wide heterozygosity) effects. We found a significant negative relationship between parental genetic relatedness and hatching success, and maternal heterozygosity was positively associated with offspring body size. The characteristics of the studied populations (recent admixture, polygynous matings) together with the fact that we found evidence for identity disequilibrium across our set of neutral markers suggest that HFCs may have resulted from genome‐wide inbreeding depression. However, one locus (Ase18) had disproportionately large effects on the observed HFCs: heterozygosity at this locus had significant positive effects on hatching success and offspring size. It suggests that this marker may lie near to a functional locus under selection (i.e. a local effect) or, alternatively, heterozygosity at this locus might be correlated to heterozygosity across the genome due to the extensive ID found in our populations (i.e. a general effect). Collectively, our results lend support to both the general and local effect hypotheses and reinforce the view that HFCs lie on a continuum from inbreeding depression to those strictly due to linkage between marker loci and genes under selection.     

SELECTION ON OVERDOMINANT GENES MAINTAINS HETEROZYGOSITY ALONG MULTIPLE CHROMOSOMES IN A CLONAL LINEAGE OF HONEY BEE

Correlations between fitness and genome‐wide heterozygosity (heterozygosity‐fitness correlations, HFCs) have been reported across a wide range of taxa. The genetic basis of these correlations is controversial: do they arise from genome‐wide inbreeding (“general effects”) or the “local effects” of overdominant loci acting in linkage disequilibrium with neutral loci? In an asexual thelytokous lineage of the Cape honey bee (Apis mellifera capensis), the effects of inbreeding have been homogenized across the population, making this an ideal system in which to detect overdominant loci, and to make inferences about the importance of overdominance on HFCs in general. Here we investigate the pattern of zygosity along two chromosomes in 42 workers from the clonal Cape honey bee population. On chromosome III (which contains the sex‐locus, a gene that is homozygous‐lethal) and chromosome IV we show that the pattern of zygosity is characterized by loss of heterozygosity in short regions followed by the telomeric restoration of heterozygosity. We infer that at least four selectively overdominant genes maintain heterozygosity on chromosome III and three on chromosome IV via local effects acting on neutral markers in linkage disequilibrium. We conclude that heterozygote advantage and local effects may be more common and evolutionarily significant than is generally appreciated.     

Molecular and pedigree measures of relatedness provide similar estimates of inbreeding depression in a bottlenecked population

Individual‐based estimates of the degree of inbreeding or parental relatedness from pedigrees provide a critical starting point for studies of inbreeding depression, but in practice wild pedigrees are difficult to obtain. Because inbreeding increases the proportion of genomewide loci that are identical by descent, inbreeding variation within populations has the potential to generate observable correlations between heterozygosity measured using molecular markers and a variety of fitness related traits. Termed heterozygosity‐fitness correlations (HFCs), these correlations have been observed in a wide variety of taxa. The difficulty of obtaining wild pedigree data, however, means that empirical investigations of how pedigree inbreeding influences HFCs are rare. Here, we assess evidence for inbreeding depression in three life‐history traits (hatching and fledging success and juvenile survival) in an isolated population of Stewart Island robins using both pedigree‐ and molecular‐derived measures of relatedness. We found results from the two measures were highly correlated and supported evidence for significant but weak inbreeding depression. However, standardized effect sizes for inbreeding depression based on the pedigree‐based kin coefficients (k) were greater and had smaller standard errors than those based on molecular genetic measures of relatedness (RI), particularly for hatching and fledging success. Nevertheless, the results presented here support the use of molecular‐based measures of relatedness in bottlenecked populations when information regarding inbreeding depression is desired but pedigree data on relatedness are unavailable.     

Evidence of opposing fitness effects of parental heterozygosity and relatedness in a critically endangered marine turtle?

How individual genetic variability relates to fitness is important in understanding evolution and the processes affecting populations of conservation concern. Heterozygosity–fitness correlations (HFCs) have been widely used to study this link in wild populations, where key parameters that affect both variability and fitness, such as inbreeding, can be difficult to measure. We used estimates of parental heterozygosity and genetic similarity (‘relatedness’) derived from 32 microsatellite markers to explore the relationship between genetic variability and fitness in a population of the critically endangered hawksbill turtle, Eretmochelys imbricata. We found no effect of maternal MLH (multilocus heterozygosity) on clutch size or egg success rate, and no single‐locus effects. However, we found effects of paternal MLH and parental relatedness on egg success rate that interacted in a way that may result in both positive and negative effects of genetic variability. Multicollinearity in these tests was within safe limits, and null simulations suggested that the effect was not an artefact of using paternal genotypes reconstructed from large samples of offspring. Our results could imply a tension between inbreeding and outbreeding depression in this system, which is biologically feasible in turtles: female‐biased natal philopatry may elevate inbreeding risk and local adaptation, and both processes may be disrupted by male‐biased dispersal. Although this conclusion should be treated with caution due to a lack of significant identity disequilibrium, our study shows the importance of considering both positive and negative effects when assessing how variation in genetic variability affects fitness in wild systems.     

A quantitative review of heterozygosity–fitness correlations in animal populations

The ease of obtaining genotypic data from wild populations has renewed interest in the relationship between individual genetic diversity and fitness-related traits (heterozygosity–fitness correlations, or HFC). Here we present a comprehensive meta-analysis of HFC studies using powerful multivariate techniques which account for nonindependence of data. We compare these findings with those from univariate techniques, and test the influence of a range of factors hypothesized to influence the strength of HFCs. We found small but significantly positive effect sizes for life-history, morphological, and physiological traits; while theory predicts higher mean effect sizes for life-history traits, effect size did not differ consistently with trait type. Newly proposed measures of variation were no more powerful at detecting relationships than multilocus heterozygosity, and populations predicted to have elevated inbreeding variance did not exhibit higher mean effect sizes. Finally, we found evidence for publication bias, with studies reporting weak, nonsignificant effects being under-represented in the literature. In general, our review shows that HFC studies do not generally reveal patterns predicted by population genetic theory, and are of small effect (less than 1% of the variance in phenotypic characters explained). Future studies should use more genetic marker data and utilize sampling designs that shed more light on the biological mechanisms that may modulate the strength of association, for example by contrasting the strength of HFCs in mainland and island populations of the same species, investigating the role of environmental stress, or by considering how selection has shaped the traits under investigation.     

Estimating genome-wide heterozygosity: effects of demographic history and marker type

Heterozygosity–fitness correlations (HFCs) are often used to link individual genetic variation to differences in fitness. However, most studies examining HFCs find weak or no correlations. Here, we derive broad theoretical predictions about how many loci are needed to adequately measure genomic heterozygosity assuming different levels of identity disequilibrium (ID), a proxy for inbreeding. We then evaluate the expected ability to detect HFCs using an empirical data set of 200 microsatellites and 412 single nucleotide polymorphisms (SNPs) genotyped in two populations of bighorn sheep (Ovis canadensis), with different demographic histories. In both populations, heterozygosity was significantly correlated across marker types, although the strength of the correlation was weaker in a native population compared with one founded via translocation and later supplemented with additional individuals. Despite being bi-allelic, SNPs had similar correlations to genome-wide heterozygosity as microsatellites in both populations. For both marker types, this association became stronger and less variable as more markers were considered. Both populations had significant levels of ID; however, estimates were an order of magnitude lower in the native population. As with heterozygosity, SNPs performed similarly to microsatellites, and precision and accuracy of the estimates of ID increased as more loci were considered. Although dependent on the demographic history of the population considered, these results illustrate that genome-wide heterozygosity, and therefore HFCs, are best measured by a large number of markers, a feat now more realistically accomplished with SNPs than microsatellites.     

Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals

Numerous studies have reported correlations between the heterozygosity of genetic markers and fitness. These heterozygosity–fitness correlations (HFCs) play a central role in evolutionary and conservation biology, yet their mechanistic basis remains open to debate. For example, fitness associations have been widely reported at both neutral and functional loci, yet few studies have directly compared the two, making it difficult to gauge the relative contributions of genome‐wide inbreeding and specific functional genes to fitness. Here, we compared the effects of neutral and immune gene heterozygosity on death from bacterial infection in Antarctic fur seal (Arctocephalus gazella) pups. We specifically developed a panel of 13 microsatellites from expressed immune genes and genotyped these together with 48 neutral loci in 234 individuals, comprising 39 pups that were classified at necropsy as having most likely died of bacterial infection together with a five times larger matched sample of healthy surviving pups. Identity disequilibrium quantified from the neutral markers was positive and significant, indicative of variance in inbreeding within the study population. However, multilocus heterozygosity did not differ significantly between healthy and infected pups at either class of marker, and little evidence was found for fitness associations at individual loci. These results support a previous study of Antarctic fur seals that found no effects of heterozygosity at nine neutral microsatellites on neonatal survival and thereby help to refine our understanding of how HFCs vary across the life cycle. Given that nonsignificant HFCs are underreported in the literature, we also hope that our study will contribute toward a more balanced understanding of the wider importance of this phenomenon.     

Heterozygosity-fitness correlations in the gilthead sea bream Sparus aurata using microsatellite loci from unknown and gene-rich genomic locations

Heterozygosity-fitness correlations (HFC) were assessed for a sample of a gilthead sea bream Sparus aurata population. Two hundred and seventy-one fish were genotyped at 22 known and novel microsatellite loci, from which correlations between the multilocus heterozygosity index (I(MLH) ) and various fitness traits (fork length, mass and specific growth rates) were calculated. Significant global HFCs were found in this sample (0·02 ≤r(2) ≤ 0·08). In addition, all the significant correlations found in this work were negative, indicating that heterozygotes had lower fitness than their homozygote counterparts. Marker location could not explain the observed HFCs. Evidence of inbreeding, outbreeding or population and family structuring was not found in this work. The presence of undetected general effects that may lead to the appearance of HFCs, however, cannot be ruled out. These results seem to be best explained by the occurrence of local effects (due to linkage) or even by possible direct locus advantages.     

Recent admixture generates heterozygosity–fitness correlations during the range expansion of an invading species

Admixture, the mixing of historically isolated gene pools, can have immediate consequences for the genetic architecture of fitness traits. Admixture may be especially important for newly colonized populations, such as during range expansion and species invasions, by generating heterozygosity that can boost fitness through heterosis. Despite widespread evidence for admixture during species invasions, few studies have examined the demographic history leading to admixture, how admixture affects the heterozygosity and fitness of invasive genotypes, and whether such fitness effects are maintained through time. We address these questions using the invasive plant Silene vulgaris, which shows evidence of admixture in both its native Europe and in North America where it has invaded. Using multilocus genotype data in conjunction with approximate Bayesian computation analysis of demographic history, we showed that admixture during the invasion of North America was independent from and much younger than admixture in the native range of Europe. We tested for fitness consequences of admixture in each range and detected a significant positive heterozygosity–fitness correlation (HFC) in North America; in contrast, no HFC was present in Europe. The lack of HFC in Europe may reflect the longer time since admixture in the native range, dissipating associations between heterozygosity at markers and fitness loci. Our results support a key short‐term role for admixture during the early stages of invasion by generating HFCs that carry populations past the threat of extinction from inbreeding and demographic stochasticity.     

Heterozygosity-fitness correlations within inbreeding classes: local or genome-wide effects?

Marker-based studies of inbreeding may lead to an enhanced understanding of inbreeding depression in natural populations, which is a major concern in conservation genetics. Correlations between marker heterozygosity and variation in fitness-associated traits—‘heterozygosity-fitness correlations’ (HFCs)—are of particular importance and have been widely applied in natural populations. In partially inbred populations, HFCs can be driven by selection against inbred individuals and thus reflect inbreeding depression. However, other explanations for HFCs also exist, such as functional effects of the markers per se or that the markers reveal selection on linked fitness genes due to extended linkage disequilibrium (LD) in the population. Accordingly, HFCs do not only arise in partially inbred populations, they may also occur within inbreeding classes such as families, i.e. in situations when there is no variation in the inbreeding coefficient. In this study we focus on the importance of LD for within-family HFCs, thereby aiming at enhancing our general understanding of HFCs. For non-coding markers, within-family HFCs have been proposed to be caused in two ways: either by ‘local effects’ at linked fitness genes in LD with the markers, or by ‘general effects’ due to a correlation between proportion of heterozygous markers (H _M ) and heterozygosity at genome-wide distributed fitness genes (H _GW ). To evaluate these contrasting hypotheses for within-family HFCs, we analysed simulated data sets of sexually reproducing populations with varying levels of LD. The results confirmed that segregation induces variation in both H _M and H _GW at a fixed level of inbreeding; as expected, the variation in H _M declined with increasing number of markers, whereas the variation in H _GW declined with decreasing LD. However, less intuitively, there was no positive correlation between the variation in H _M and H _GW within inbreeding classes when the local component of H _GW was accounted for (i.e. when the part of the chromosome in LD with the markers was excluded). This strongly suggests that within-family HFCs are not caused by general effects. Instead, our results support the idea that HFCs at a known level of inbreeding can be driven by local effects in populations with high to moderate LD. Note however that we define the local component of H _GW as the part of the chromosomes in LD with the markers. This implies that when LD is high, the local component will consist of a substantial part of the genome and thus provides a rather ‘genome-wide’ view. We caution against routinely interpreting positive HFCs as evidence of inbreeding depression and non-significant HFCs as lack thereof, especially when few markers are used.     

Effects of inbreeding on fitness‐related traits in a small isolated moose population

Inbreeding can affect fitness‐related traits at different life history stages and may interact with environmental variation to induce even larger effects. We used genetic parentage assignment based on 22 microsatellite loci to determine a 25 year long pedigree for a newly established island population of moose with 20–40 reproducing individuals annually. We used the pedigree to calculate individual inbreeding coefficients and examined for effects of individual inbreeding (f) and heterozygosity on fitness‐related traits. We found negative effects of f on birth date, calf body mass and twinning rate. The relationship between f and calf body mass and twinning rate were found to be separate but weaker after accounting for birth date. We found no support for an inbreeding effect on the age‐specific lifetime reproductive success of females. The influence of f on birth date was related to climatic conditions during the spring prior to birth, indicating that calves with a low f were born earlier after a cold spring than calves with high f. In years with a warm spring, calf f did not affect birth date. The results suggest that severe inbreeding in moose has both indirect effects on fitness through delayed birth and lower juvenile body mass, as well as separate direct effects, as there still was a significant relationship between f and twinning rate after accounting for birth date and body mass as calf. Consequently, severe inbreeding as found in the study population may have consequences for population growth and extinction risk.