Estimated Breeding Values for Canine Hip Dysplasia Radiographic Traits in a Cohort of Australian German Shepherd Dogs

Canine hip dysplasia (CHD) is a serious and common musculoskeletal disease of pedigree dogs and therefore represents both an important welfare concern and an imperative breeding priority. The typical heritability estimates for radiographic CHD traits suggest that the accuracy of breeding dog selection could be substantially improved by the use of estimated breeding values (EBVs) in place of selection based on phenotypes of individuals. The British Veterinary Association/Kennel Club scoring method is a complex measure composed of nine bilateral ordinal traits, intended to evaluate both early and late dysplastic changes. However, the ordinal nature of the traits may represent a technical challenge for calculation of EBVs using linear methods. The purpose of the current study was to calculate EBVs of British Veterinary Association/Kennel Club traits in the Australian population of German Shepherd Dogs, using linear (both as individual traits and a summed phenotype), binary and ordinal methods to determine the optimal method for EBV calculation. Ordinal EBVs correlated well with linear EBVs (r = 0.90–0.99) and somewhat well with EBVs for the sum of the individual traits (r = 0.58–0.92). Correlation of ordinal and binary EBVs varied widely (r = 0.24–0.99) depending on the trait and cut-point considered. The ordinal EBVs have increased accuracy (0.48–0.69) of selection compared with accuracies from individual phenotype-based selection (0.40–0.52). Despite the high correlations between linear and ordinal EBVs, the underlying relationship between EBVs calculated by the two methods was not always linear, leading us to suggest that ordinal models should be used wherever possible. As the population of German Shepherd Dogs which was studied was purportedly under selection for the traits studied, we examined the EBVs for evidence of a genetic trend in these traits and found substantial genetic improvement over time. This study suggests the use of ordinal EBVs could increase the rate of genetic improvement in this population.     

Genetic Correlations among Canine Hip Dysplasia Radiographic Traits in a Cohort of Australian German Shepherd Dogs,and Implications for the Design of a More Effective Genetic Control Program

Canine hip dysplasia (CHD) is a common musculoskeletal disease in pedigree dog populations. It can cause severe pain and dysfunction which may require extensive medication and/or surgical treatment and often ultimately requires humane euthanasia. CHD has been found to be moderately heritable and, given its impact on welfare, should be considered an imperative breeding priority. The British Veterinary Association/Kennel Club scoring method is one of several measures used to assess the genetic propensity of potential breeding stock for dysplastic changes to the hips based on radiographic examination. It is a complex measure composed of nine ordinal traits, intended to evaluate both early and late dysplastic changes. It would be highly desirable if estimated breeding values (EBVs) for these nine traits were consolidated into a simpler, EBV-based, selection index more easily usable by breeders. A multivariate analysis on the phenotype scores from an Australian cohort of 13,124 German Shepherd Dogs (GSDs) returned genetic correlations between 0.48–0.97 for the nine traits which fell into two trait groups, Group 1 reflecting early changes (“laxity”) and Group 2 reflecting late changes (“osteoarthritis”). Principal components analysis of the ordinal EBVs suggested the same pattern, with strong differentiation between “laxity” and “osteoarthritis” traits in the second component. Taking account of all results, we recommend interim use of two selection indexes: the first being the average of ordinal EBVs for “laxity” traits and the second being the average of ordinal EBVs for “osteoarthritis” traits. The correlation between these two selection indexes (0.771–0.774) is sufficiently less than unity enabling the selection of dogs with different genetic propensity for laxity and for osteoarthritic CHD changes in GSDs; this may also be applicable in other breeds. Dogs with low propensity for severe osteoarthritic change in the presence of laxity may be of interest both in molecular research and breeding programs.     

Retrospective Analysis for Genetic Improvement of Hip Joints of Cohort Labrador Retrievers in the United States: 1970–2007

Background

Canine Hip Dysplasia (CHD) is a common inherited disease that affects dog wellbeing and causes a heavy financial and emotional burden to dog owners and breeders due to secondary hip osteoarthritis. The Orthopedic Foundation for Animals (OFA) initiated a program in the 1960''s to radiograph hip and elbow joints and release the OFA scores to the public for breeding dogs against CHD. Over last four decades, more than one million radiographic scores have been released.

Methodology/Principal Findings

The pedigrees in the OFA database consisted of 258,851 Labrador retrievers, the major breed scored by the OFA (25% of total records). Of these, 154,352 dogs had an OFA hip score reported between 1970 and 2007. The rest of the dogs (104,499) were the ancestors of the 154,352 dogs to link the pedigree relationships. The OFA hip score is based on a 7-point scale with the best ranked as 1 (excellent) and the worst hip dysplasia as 7. A mixed linear model was used to estimate the effects of age, sex, and test year period and to predict the breeding value for each dog. Additive genetic and residual variances were estimated using the average information restricted maximum likelihood procedure. The analysis also provided an inbreeding coefficient for each dog. The hip scores averaged 1.93 (±SD = 0.59) and the heritability was 0.21. A steady genetic improvement has accrued over the four decades. The breeding values decreased (improved) linearly. By the end of 2005, the total genetic improvement was 0.1 units, which is equivalent to 17% of the total phenotypic standard deviation.

Conclusion/Significance

A steady genetic improvement has been achieved through the selection based on the raw phenotype released by the OFA. As the heritability of the hip score was on the low end (0.21) of reported ranges, we propose that selection based on breeding values will result in more rapid genetic improvement than breeding based on phenotypic selection alone.     

Genetic parameters for agronomic characteristics. I. Early and intermediate breeding populations of true potato seed

The original variation in the source population as well as the selection method may influence the genetic variation in further cycles of genetic improvement. Therefore, the objectives of this research were to determine genetic parameters (variance components and heritability) in source and intermediate stages of a true potato seed (TPS) breeding population and to calculate the genetic and phenotypic correlations in this breeding material developed by the Centro Internacional de la Papa (CIP). The intermediate stage was derived from a source population adapted to the warm lowland tropics plus introduction of exotic germplasm from North America and Europe. Non-additive genetic variation was almost nil for plant survival, tuber yield and tuber shape uniformity in both stages of the breeding population and no quantitative genetic variation for uniformity of tuber color was observed in both source and intermediate breeding materials. Heritability was higher in the intermediate stage than in the source population for plant survival (0.86 vs 0.66), tuber yield (0.30 vs 0.14) and tuber shape (0.77 vs 0.51), but it was the reverse for tuber uniformity (0.11 vs 0.72). These results suggest that potato breeders at CIP were able to keep enough genetic variation for most important characteristics for potato production from true seed in their intermediate breeding materials by adding new sources of variation to the original breeding population. Additive genetic and phenotypic correlations were significant and positive between plant vigor after transplanting and tuber yield, and tuber shape and tuber uniformity, which suggest that high yielding offspring result from early vigorous growth, and that tuber uniformity could depend on tuber shape uniformity in this breeding material.     

Genetic evaluation of hip score in UK Labrador Retrievers

Hip dysplasia is an important and complex genetic disease in dogs with both genetic and environmental influences. Since the osteoarthritis that develops is irreversible the only way to improve welfare, through reducing the prevalence, is through genetic selection. This study aimed to evaluate the progress of selection against hip dysplasia, to quantify potential improvements in the response to selection via use of genetic information and increases in selection intensity, and to prepare for public provision of estimated breeding values (EBV) for hip dysplasia in the UK. Data consisted of 25,243 single records of hip scores of Labrador Retrievers between one and four years old, from radiographs evaluated between 2000 and 2007 as part of the British Veterinary Association (BVA) hip score scheme. A natural logarithm transformation was applied to improve normality and linear mixed models were evaluated using ASREML. Genetic correlations between left and right scores, and total hip scores at one, two and three years of age were found to be close to one, endorsing analysis of total hip score in dogs aged one to three as an appropriate approach. A heritability of 0.35±0.016 and small but significant litter effect (0.07±0.009) were estimated. The observed trends in both mean hip score and mean EBV over year of birth indicate that a small genetic improvement has been taking place, approximately equivalent to avoiding those dogs with the worst 15% of scores. Deterministic analysis supported by simulations showed that a 19% greater response could be achieved using EBV compared to phenotype through increases in accuracy alone. This study establishes that consistent but slow genetic improvement in the hip score of UK Labrador Retrievers has been achieved over the previous decade, and demonstrates that progress may be easily enhanced through the use of EBVs and more intense selection.     

Heritability in the genome-wide association era

Heritability, the fraction of phenotypic variation explained by genetic variation, has been estimated for many phenotypes in a range of populations, organisms, and time points. The recent development of efficient genotyping and sequencing technology has led researchers to attempt to identify the genetic variants responsible for the genetic component of phenotype directly via GWAS. The gap between the phenotypic variance explained by GWAS results and those estimated from classical heritability methods has been termed the "missing heritability problem". In this work, we examine modern methods for estimating heritability, which use the genotype and sequence data directly. We discuss them in the context of classical heritability methods, the missing heritability problem, and describe their implications for understanding the genetic architecture of complex phenotypes.     

Complex segregation analysis of canine hip dysplasia in German shepherd dogs

Complex segregation analyses were carried out to clarify the mode of inheritance of canine hip dysplasia (CHD) in German shepherd dogs. Data were used from 8,567 animals examined for CHD from 20 families with three to four generations. The existence of a major gene in addition to polygenic gene effects was detected. In the present study, a mixed model with a dominant major gene effect seemed to be most probable for dichotomous encoding (0: dogs without signs of CHD; 1: dogs with borderline/slight to severe CHD). In addition, mixed major gene inheritance was shown for a binary trait where borderline was assigned to dogs scored free from CHD and for a trichotomously encoded trait (0: dogs without signs of CHD; 1: borderline CHD; 2: mild to severe CHD). Although only small frequencies were found for the unfavorable homozygotic genotype AA, the probability of the AB genotype was high in affected animals. Selection schemes to reduce the frequency of the allele A should therefore efficiently improve existing breeding programmes in German shepherd dogs.     

Multiple loci associated with canine hip dysplasia (CHD) in German shepherd dogs

Canine hip dysplasia (CHD) is the most common hereditary skeletal disorder in dogs. To identify common alleles associated with CHD, we developed 37 informative single nucleotide polymorphisms (SNPs) within 13 quantitative trait loci (QTL) previously identified for German shepherd dogs. These SNPs were genotyped in 95 German shepherd dogs affected by CHD and 95 breed, sex, and birth year-matched controls. A total of ten SNPs significant at a nominal P value of 0.05 were validated in 843 German shepherd dogs including 277 unaffected dogs and 566 CHD-affected dogs. Cases and controls were sampled from the whole German shepherd dog population in Germany in such a way that mean coancestry coefficients were below 0.1 % within cases and controls as well as among cases and controls. We identified nine SNPs significantly associated with CHD within five QTL on dog chromosomes (CFA) 3, 9, 26, 33, and 34. Genotype effects of these nine SNPs explained between 22 and 34 % of the phenotypic variance of hip dysplasia in German shepherd dogs. The strongest associated SNPs were located on CFA33 and 34 within the candidate genes PNCP, TRIO, and SLC6A3. Thus, the present study validated positional candidate genes within five QTL for CHD.     

Genetic and phenotypic aspects of foot lesion scores in sheep of different breeds and ages

Footrot is a costly endemic disease of sheep. This study investigates the potential to decrease its prevalence through selective breeding for decreased lesion score. Pedigreed mule and Scottish Blackface (SBF) ewes were scored for lesions on each hoof on a 0 to 4 scale for up to 2 (SBF ewes) or 4 (mules) times over 2 years. One score was obtained for SBF lambs. An animal was deemed to have lesions (severe lesions) if at least one hoof had a score of at least 1 (2). The prevalence of lesions was 34% in lambs, 17% in SBF ewes and 51% in mules. The heritability of lesions (severe lesions) analysed as repeated measurements of the same trait in a threshold model was 0.19 (0.26) in SBF ewes and 0.12 (0.19) in mules. Estimates for the sum and maximum of scores as well as the number of feet affected were much lower, as were estimates for permanent animal effects (i.e. non-genetic effects associated with an animal). When successive scores on the same animal were analysed as correlated traits, heritability estimates for most traits tended to be higher, except for severe footrot in mules where estimates varied greatly over time. The phenotypic correlations between successive scores in SBF ewes were close to 0, genetic correlations were moderately positive (0.18 to 0.55). Correlations in mules were generally of a similar size, but some genetic correlations were higher (up to 0.92). There was a clear trend for heritabilities for lesions and severe lesions to increase with higher prevalence of lesions, even when analysed in a threshold model. Heritability estimates for traits that combine scores over several events in mules, identifying the more persistently affected animals, ranged from 0.12 to 0.23 with the highest estimates for the average number of feet that were (severely) affected in animals scored for a minimum at two events. The heritability of all lesion traits in lambs was estimated as 0. It is concluded that selection for lower lesions is possible in ewes but not lambs, and that a simple binary score at an animal level is at least as effective as a comprehensive score at hoof level. Given the low repeatability of lesion scores, repeated measures over time will improve effectiveness of selection. Selection across environments (flocks, seasons) with different prevalences of lesions scores will need to take account of variation in the heritability.     

Identification and Validation of Quantitative Trait Loci (QTL) for Canine Hip Dysplasia (CHD) in German Shepherd Dogs

Canine hip dysplasia (CHD) is the most common hereditary skeletal disorder in dogs. To identify common alleles associated with CHD, we genotyped 96 German Shepherd Dogs affected by mild, moderate and severe CHD and 96 breed, sex, age and birth year matched controls using the Affymetrix canine high density SNP chip. A mixed linear model analysis identified five SNPs associated with CHD scores on dog chromosomes (CFA) 19, 24, 26 and 34. These five SNPs were validated in a by sex, age, birth year and coancestry stratified sample of 843 German Shepherd Dogs including 277 unaffected dogs and 566 CHD-affected dogs. Mean coancestry coefficients among and within cases and controls were <0.1%. Genotype effects of these SNPs explained 20–32% of the phenotypic variance of CHD in German Shepherd Dogs employed for validation. Genome-wide significance in the validation data set could be shown for each one CHD-associated SNP on CFA24, 26 and 34. These SNPs are located within or in close proximity of genes involved in bone formation and related through a joint network. The present study validated positional candidate genes within two previously known quantitative trait loci (QTL) and a novel QTL for CHD in German Shepherd Dogs.     

Heritability of flight and resting metabolic rates in the Glanville fritillary butterfly

Dispersal capacity is a key life‐history trait especially in species inhabiting fragmented landscapes. Evolutionary models predict that, given sufficient heritable variation, dispersal rate responds to natural selection imposed by habitat loss and fragmentation. Here, we estimate phenotypic variance components and heritability of flight and resting metabolic rates (RMRs) in an ecological model species, the Glanville fritillary butterfly, in which flight metabolic rate (FMR) is known to correlate strongly with dispersal rate. We modelled a two‐generation pedigree with the animal model to distinguish additive genetic variance from maternal and common environmental effects. The results show that FMR is significantly heritable, with additive genetic variance accounting for about 40% of total phenotypic variance; thus, FMR has the potential to respond to selection on dispersal capacity. Maternal influences on flight metabolism were negligible. Heritability of flight metabolism was context dependent, as in stressful thermal conditions, environmentally induced variation dominated over additive genetic effects. There was no heritability in RMR, which was instead strongly influenced by maternal effects. This study contributes to a mechanistic understanding of the evolution of dispersal‐related traits, a pressing question in view of the challenges posed to many species by changing climate and fragmentation of natural habitats.     

都市园林植物云南樱花的表型多样性研究

云南樱花(Prunus yunnannensis)为蔷薇科(Rosaceae)多年生落叶乔木,是中国西南地区特有的重要园林观赏植物,其在昆明园林绿化中具有较高的应用价值。以昆明地区的云南樱花为研究对象,研究了6个栽培居群120个单株的16个表型性状的多样性,分析了16个表型性状的相关性和广义遗传力,并对6个栽培居群进行了聚类分析,旨在探明其在资源应用过程中的表型变异程度及变异规律,为今后优良性状选育与种质推广提供科学依据。结果表明:云南樱花在居群间及居群内均存在丰富的表型多样性,除雌蕊长以外,其它15个表型性状在各居群之间均存在显著性差异,其中各性状的平均变异幅度为7.73%~94.04%,在居群内的变异幅度为20.74%~28.22%,各性状居群内的变异明显小于居群间,16个表型性状的广义遗传力介于0.54~0.97之间,其中叶长的广义遗传力最大,而雌蕊长的广义遗传力最小。对云南樱花16个形态指标的相关性分析表明,大部分形态指标之间均存在显著的相关性。利用居群间欧氏距离进行的UPGMA聚类分析结果表明,云南樱花6个栽培居群可以聚为2类。     

Variation in heritability of tadpole growth: an experimental analysis

Heritability characteristically shows large variation between traits, among populations and species, and through time. One of the reasons for this is its dependence on gene frequencies and how these are altered by selection and drift through the evolutionary process. We studied variation in heritability of tadpole growth rate in populations of the Swedish common frog, Rana temporaria. In populations evolving under warmer conditions, we have demonstrated elsewhere that tadpoles show better growth and physiological performance at relatively higher temperatures than tadpoles with an evolutionary history in a relatively cooler part of the distribution range. In the current study, we ask whether this process of divergence under natural selection has influenced the genetic architecture as visualised in estimates of heritability of growth rate at different temperature treatments under laboratory conditions. The results suggest that the additive genetic variance varies between treatments and is highest in a treatment that is common to both populations. Our estimates of narrow sense heritability are generally higher in the thermal regime that dominates in the natural environment. The reason for this appears not primarily to be because the component of additive genetic variation is higher in relation to the total phenotypic variation under these conditions, but because the part of the phenotypic variance explained by environmental variation increases at temperatures to which the current populations has been less frequently under selection.     

A test of quantitative genetic theory using Drosophila- effects of inbreeding and rate of inbreeding on heritabilities and variance components

Inbreeding is expected to decrease the heritability within populations. However, results from empirical studies are inconclusive. In this study, we investigated the effects of three breeding treatments (fast and slow rate of inbreeding - inbred to the same absolute level - and a control) on heritability, phenotypic, genetic and environmental variances of sternopleural bristle number in Drosophila melanogaster. Heritability, and phenotypic, genetic and environmental variances were estimated in 10 replicate lines within each of the three treatments. Standard least squares regression models and Bayesian methods were used to analyse the data. Heritability and additive genetic variance within lines were higher in the control compared with both inbreeding treatments. Heritabilities and additive genetic variances within lines were higher in slow compared with fast inbred lines, indicating that slow inbred lines retain more evolutionary potential despite the same expected absolute level of inbreeding. The between line variance was larger with inbreeding and more than twice as large in the fast than in the slow inbred lines. The different pattern of redistribution of genetic variance within and between lines in the two inbred treatments cannot be explained invoking the standard model based on selective neutrality and additive gene action. Environmental variances were higher with inbreeding, and more so with fast inbreeding, indicating that inbreeding and the rate of inbreeding affect environmental sensitivity. The phenotypic variance decreased with inbreeding, but was not affected by the rate of inbreeding. No inbreeding depression for mean sternopleural bristle number was observed in this study. Considerable variance between lines in additive genetic variance within lines was observed, illustrating between line variation in evolutionary potential.     

Heritability and Y-chromosome influence in the jack male life history of chinook salmon (Oncorhynchus tshawytscha)

Jacking in chinook salmon (Oncorhynchus tshawytscha) is an alternative reproductive strategy in which males sexually mature at least 1 year before other members of their year class. We characterize the genetic component of this reproductive strategy using two approaches; hormonal phenotypic sex manipulation, and a half-sib breeding experiment. We 'masculinized' chinook salmon larvae with testosterone, reared them to first maturation, identified jacks and immature males based on phenotype, and genotyped all fish as male ('XY') or female ('XX') using PCR-based Y-chromosome markers. The XY males had a much higher incidence of jacking than the XX males (30.8% vs 9.9%). There was no difference in body weight, gonad weight, and plasma concentrations of testosterone and 17beta-estradiol between the two jack genotypes, although XY jacks did have a higher gonadosomatic index (GSI) than XX jacks. In the second experiment, we bred chinook salmon in two modified half-sib mating designs, and scored the number of jacks and immature fish at first maturation. Heritability of jacking was estimated using two ANOVA models: dams nested within sires, and sires nested within dams with one-half of the half-sib families common to the two models. The sire component of the additive genetic variance yielded a high heritability estimate and was significantly higher than the dam component (h(2)(sire) = 0.62 +/- 0.21; h(2)(dam) = -0.14 +/- 0.12). Our experiments both indicated a strong sex-linked component (Y-chromosome) to jacking in chinook salmon, although evidence for at least some autosomal contribution was also observed.     

Robust modeling of additive and nonadditive variation with intuitive inclusion of expert knowledge

We propose a novel Bayesian approach that robustifies genomic modeling by leveraging expert knowledge (EK) through prior distributions. The central component is the hierarchical decomposition of phenotypic variation into additive and nonadditive genetic variation, which leads to an intuitive model parameterization that can be visualized as a tree. The edges of the tree represent ratios of variances, for example broad-sense heritability, which are quantities for which EK is natural to exist. Penalized complexity priors are defined for all edges of the tree in a bottom-up procedure that respects the model structure and incorporates EK through all levels. We investigate models with different sources of variation and compare the performance of different priors implementing varying amounts of EK in the context of plant breeding. A simulation study shows that the proposed priors implementing EK improve the robustness of genomic modeling and the selection of the genetically best individuals in a breeding program. We observe this improvement in both variety selection on genetic values and parent selection on additive values; the variety selection benefited the most. In a real case study, EK increases phenotype prediction accuracy for cases in which the standard maximum likelihood approach did not find optimal estimates for the variance components. Finally, we discuss the importance of EK priors for genomic modeling and breeding, and point to future research areas of easy-to-use and parsimonious priors in genomic modeling.     

Maintenance of genetic variation in quantitative traits of a woodland rodent during generations of captive breeding

Breeding programs to conserve diversity are predicated on the assumption that genetic variation in adaptively important traits will be lost in parallel to the loss of variation at neutral loci. To test this assumption, we monitored quantitative traits across 18 generations of Peromyscus leucopus mice propagated with protocols that mirror breeding programs for threatened species. Ears, hind feet, and tails became shorter, but changes were reversible by outcrossing and therefore were due to accumulated inbreeding. Heritability of ear length decreased, because of an increase in phenotypic variance rather than the expected decrease in additive genetic variance. Additive genetic variance in hind foot length increased. This trait initially had low heritability but large dominance or common environmental variance contributing to resemblance among full-sibs. The increase in the additive component indicates that there was conversion of interaction variances to additive variance. For no trait did additive genetic variation decrease significantly across generations. These findings indicate that the restructuring of genetic variance that occurs with genetic drift and novel selection in captivity can prevent or delay the loss of phenotypic and heritable variation, providing variation on which selection can act to adapt populations to captivity and perhaps later to readapt to more natural habitats after release. Therefore, the importance of minimizing loss of gene diversity from conservation breeding programs for threatened wildlife species might lie in preventing immediate reduction in individual fitness due to inbreeding and protecting allelic diversity for long-term evolutionary change, more so than in protecting variation in quantitative traits for rapid re-adaptation to wild environments.     

Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection

Variation among females in mate choice may influence evolution by sexual selection. The genetic basis of this variation is of interest because the elaboration of mating preferences requires additive genetic variation in these traits. Here we measure the repeatability and heritability of two components of female choosiness (responsiveness and discrimination) and of female preference functions for the multiple ornaments borne by male guppies (Poecilia reticulata). We show that there is significant repeatable variation in both components of choosiness and in some preference functions but not in others. There appear to be several male ornaments that females find uniformly attractive and others for which females differ in preference. One consequence is that there is no universally attractive male phenotype. Only responsiveness shows significant additive genetic variation. Variation in responsiveness appears to mask variation in discrimination and some preference functions and may be the most biologically relevant source of phenotypic and genetic variation in mate-choice behavior. To test the potential evolutionary importance of the phenotypic variation in mate choice that we report, we estimated the opportunity for and the intensity of sexual selection under models of mate choice that excluded and that incorporated individual female variation. We then compared these estimates with estimates based on measured mating success. Incorporating individual variation in mate choice generally did not predict the outcome of sexual selection any better than models that ignored such variation.     

Variation in heritability of immune function in the tree swallow

Heritability is an important component of the ability of a trait to respond to natural selection; variation in heritability can lead to differences in how a trait responds to selection pressures. Here we test whether an important physiological trait, immune function, varies by comparing heritability estimates through cross-fostering brood manipulation at three wide-spread sites in the tree swallow (Tachycineta bicolor): Alaska, New York and Tennessee. In two of three sites, there was no additive genetic component to nestling immune response to the mitogen phytohaemagglutinin, while immune response had a heritable component in Tennessee. Bootstrapping revealed significant differences in estimated heritability. This conclusion was supported by mother–offspring regressions; in Tennessee breeding females mounting strong immune responses tended to have offspring with strong immune responses, while in New York and Alaska, there was no relationship between the immune responses of mothers and offspring. These results suggest that studies investigating the roles of common origin and rearing environment should consider yearly or spatial variation within a species.