THE EFFECT OF ENVIRONMENTAL VARIABILITY ON THE HERITABILITIES OF TRAITS OF A FIELD CRICKET

The presence of heritable variation in traits is a prerequisite for evolution. The great majority of heritability (h²) estimates are performed under laboratory conditions that are characterized by low levels of environmental variability. Very little is known about the effect of environmental variability on the estimation of components of quantitative variation, although theoretical extrapolations from lab studies have been attempted. Here we investigate the effects of environmental heterogeneity on variance component estimation using full-sib families of Gryllus pennsylvanicus split between a homogeneous laboratory environment and a more variable field environment. Although large standard errors prevent demonstration of statistically significant differences among h² of traits measured in the two environments for all but one trait, the values of h² are, on average, lower in the variable field environment, with a mean reduction of 19%. Developmental time is an exception, exhibiting high levels of additive variance in the field, leading to a higher value of h² in the variable environment. Underlying the lower field h² estimates are greater components of environmental variance as expected, as well as lower components of genetic variance. In this study, there is no evidence that the increase in the environmental component of variance in the field is any more important in the reduction of h² than is the decrease in the additive genetic component. The implications of the relative changes in the two components of variance are discussed.     

The effect of trait type and strength of selection on heritability and evolvability in an island bird population

The heritability (h²) of fitness traits is often low. Although this has been attributed to directional selection having eroded genetic variation in direct proportion to the strength of selection, heritability does not necessarily reflect a trait's additive genetic variance and evolutionary potential (“evolvability”). Recent studies suggest that the low h² of fitness traits in wild populations is caused not by a paucity of additive genetic variance (V_A) but by greater environmental or nonadditive genetic variance (V_R). We examined the relationship between h² and variance‐standardized selection intensities (i or β_σ), and between evolvability (I_A:V_A divided by squared phenotypic trait mean) and mean‐standardized selection gradients (β_μ). Using 24 years of data from an island population of Savannah sparrows, we show that, across diverse traits, h² declines with the strength of selection, whereas I_A and I_R (V_R divided by squared trait mean) are independent of the strength of selection. Within trait types (morphological, reproductive, life‐history), h², I_A, and I_R are all independent of the strength of selection. This indicates that certain traits have low heritability because of increased residual variance due to the age at which they are expressed or the multiple factors influencing their expression, rather than their association with fitness.     

Genetic Variability of Adult Body Mass Index: A Longitudinal Assessment in Framingham Families

Objective: To explore the contribution of genetics to the mean, SD, maximum value, maximum less the mean, and change over time in body mass index (BMI) and the residual of body weight after adjustment for height. BMI is frequently used as a general indicator of obesity because of its ease and reliability in ascertainment. Cross‐sectional twin and family studies have shown a moderate‐to‐substantial genetic component for BMI. However, the contribution of genetics to the long‐term average, variability, or change over time in BMI is less clear. Research Methods and Procedures: Longitudinal data from the Framingham heart study were used to create pedigrees of age‐matched individuals. Heritability estimates were derived using variance‐decomposition methods on a total of 1051 individuals from 380 extended pedigrees followed for a period of 20 years. All subjects were followed from approximately age 35 to 55 years. Results: Moderate heritability estimates were found for the mean BMI (h² = 0.37), maximum BMI (h² = 0.40), and the mean residual of body weight (h² = 0.36). Low heritability estimates (h² ? 0.20) were found for the maximum less the mean in BMI and the SDs of BMI and residual of body weight. No additive genetic contribution was found for the average change over time in BMI or the residual of body weight. Discussion: These findings suggest that there is a significant genetic component for the magnitude of BMI throughout an individual's middle‐adult years; however, little evidence was found for a genetic contribution to the variability or rate of change in an individual's BMI.     

Environmental and genetic influences on body mass and resting metabolic rates (RMR) in a natural population of weasel Mustela nivalis

Body mass (BM) and resting metabolic rates (RMR) are two inexorably linked traits strongly related to mammalian life histories. Yet, there have been no studies attempting to estimate heritable variation and covariation of BM and RMR in natural populations. We used a marker‐based approach to construct a pedigree and then the ‘animal model’ to estimate narrow sense heritability (h²) of these traits in a free‐living population of weasels Mustela nivalis—a small carnivore characterised by a wide range of BM and extremely high RMR. The most important factors affecting BM of weasels were sex and habitat type, whereas RMR was significantly affected only by seasonal variation of this trait. All environmental factors had only small effect on estimates of additive genetic variance of both BM and RMR. The amount of additive genetic variance associated with BM and estimates of heritability were high and significant in males (h² = 0.61), but low and not significant in females (h² = 0.32), probably due to small sample size for the latter sex. The results from the two‐trait model revealed significant phenotypic (r_P = 0.62) and genetic correlation (r_A = 0.89) between BM and whole body RMR. The estimate of heritability of whole body RMR (0.54) and BM corrected RMR (0.45) were lower than estimates of heritability for BM. Both phenotypic and genetic correlations between BM corrected RMR and BM had negative signals (r_P = ?0.42 and r_A = ?0.58). Our results indicate that total energy expenditures of individuals can quickly evolve through concerted changes in BM and RMR.     

Heritability of resistance to oxidative stress in early life

Oxidative stress has recently been suggested to play an important role in life‐history evolution, but little is known about natural variation and heritability of this physiological trait. Here, we explore phenotypic variation in resistance to oxidative stress of cross‐fostered yellow‐legged gull (Larus cachinnans) chicks. Resistance to oxidative stress was not related to plasma antioxidants at hatching, which are mostly derived from maternal investment into eggs. Common environmental effects on phenotypic variation in resistance to oxidative stress were not significant. Heritability was relatively low and nonsignificant in hatchlings, but interestingly, the chicks of age 8 days showed high and significant heritability (h² = 0.59). Our results suggest that resistance to oxidative stress is determined mainly by the genotype as chicks grow. Further work is required to explore the genetic role of oxidative stress in life‐history evolution.     

Post‐weaning parental care increases fitness but is not heritable in North American red squirrels

Most empirical attempts to explain the evolution of parental care have focused on its costs and benefits (i.e. fitness consequences). In contrast, few investigations have been made of the other necessary prerequisite for evolutionary change, inheritance. Here, we examine the fitness consequences and heritability (h²) of a post‐weaning parental care behaviour (territory bequeathal) in a wild population of North American red squirrels. Each year, a subset (average across all years = 19%) of reproductive females bequeathed their territory to a dependent offspring. Bequeathing females experienced higher annual reproductive success and did not suffer a survival cost to themselves relative to those females retaining their territory. Bequeathing females thus realized higher relative annual fitness [ω = 1.18 ± 0.03 (SE)] than nonbequeathing females [ω = 0.96 ± 0.02 (SE)]. Additive genetic influences on bequeathal behaviour, however, were not significantly different from 0 (h² = 1.9 × 10^?3; 95% highest posterior density interval = 3.04 × 10^?8 to 0.37) and, in fact, bequeathal behaviour was not significantly repeatable (R = 2.0 × 10^?3; 95% HPD interval =0–0.27). In contrast, directional environmental influences were apparent. Females were more likely to bequeath in years following low food abundance and when food availability in the upcoming autumn was high. Despite an evident fitness benefit, a lack of heritable genetic variance will constrain evolution of this trait.     

On Probability of Heritability Estimates from Full-Sib Analysis Exceeding Unity Based on Underlying Theoretical Distribution

A procedure for obtaining the theoretical probability of heritability (h²) estimates from full-sib analysis exceeding unity is described. Probability densities useful in the evaluation of these probabilities are also derived. These are used for obtaining the probabilities for several combinations of sire/dam numbers and three levels of h² (0.10, 0.25, 0.50) assuming additive genetic model and two full-sibs per mating.     

Familial Resemblance of 7‐Year Changes in Body Mass and Adiposity

Objective: To investigate the familial resemblance of 7‐year changes in body mass and adiposity among Canadian families. Research Methods and Procedures: The sample consisted of 655 women and 660 men from 521 families who participated in the Canada Fitness Survey in 1981 and the follow‐up Campbell's Survey in 1988. Indicators of baseline and 7‐year changes in body mass and adiposity included body mass (kilograms), body mass index (BMI; kilograms per square meter), sum of five skinfolds (SF5; millimeters), and waist circumference (WC; millimeters). The data were adjusted for the effects of age and sex, and the change scores were adjusted for baseline levels. A familial correlation model was used to determine the heritability of each phenotype using maximum likelihood techniques. Results: Significant familial resemblance was observed at baseline and for 7‐year changes in all phenotypes. At baseline, moderate heritabilities were observed [body mass: heritability coefficient (h²) = 56%; BMI, h² = 39%; SF5, h² = 41%; and WC, h² = 39%], whereas values were attenuated for each change score except for WC (Δbody mass, h² = 23%; ΔBMI, h² = 14%; ΔSF5, h² = 12%; and ΔWC, h² = 45%). Discussion: Changes in body mass and adiposity significantly aggregate within families over 7 years. However, baseline values are characterized by higher heritability levels except WC. The significant heritabilities observed for change scores suggest that lifestyle, transient environmental factors, and possibly age‐related gene effects are important determinants of changes in body mass and adiposity.     

Genetic investigation of contributions of embryo and endosperm genes to malt Kolbach index, alpha-amylase activity and wort nitrogen content in barley

 A genetic model is proposed for the analysis of embryo and endosperm effects as well as GE interaction effects. An investigation of three malting quality traits in grains of seven parents and their F₂s was undertaken in a half-diallel cross of barley (Hordeum distichum L.) over 2 years. The results indicated that the malt Kolbach index (KI), alpha-amylase activity (αAA) and wort soluble nitrogen (Wort-N) are controlled by both embryo genetic effects and endosperm genetic effects. Variance of the endosperm additive effects was obviously larger than that of the embryo additive effects. In the contribution of the embryo genetic effects to variation in malt αAA and Wort-N, the dominance effects were considerably larger than the additive effects. The endosperm dominance effects constituted a major part of the total genetic effect on the KI. Significant endosperm GE interactions were also detected in the malt traits concerned. Endosperm general heritability (h ² _e ) tended to be larger than interaction heritability (h ² _oE or h ² _eE ) for all the traits. Endosperm heterosis was observed to be significantly positive for αAA but negative for Wort-N in the F₂ seed generation. Prediction of main gene effects for seven parents showed that ‘Ganmu 2’ and ‘Supi1’ were suitable parental varieties for malt αAA and Wort-N improvement. Our genetic model for malting quality traits and its application in breeding are discussed. Received: 5 August 1997 / Accepted: 11 September 1997     

Heritability of anti‐predatory traits: vigilance and locomotor performance in marmots

Animals must allocate some proportion of their time to detecting predators. In birds and mammals, such anti‐predator vigilance has been well studied, and we know that it may be influenced by a variety of intrinsic and extrinsic factors. Despite hundreds of studies focusing on vigilance and suggestions that there are individual differences in vigilance, there have been no prior studies examining its heritability in the field. Here, we present one of the first reports of (additive) genetic variation in vigilance. Using a restricted maximum likelihood procedure, we found that, in yellow‐bellied marmots (Marmota flaviventris), the heritability of locomotor ability (h² = 0.21), and especially vigilance (h² = 0.08), is low. These modest heritability estimates suggest great environmental variation or a history of directional selection eliminating genetic variation in these traits. We also found a significant phenotypic (r_P = ?0.09 ± 0.04, P = 0.024) and a substantial, but not significant, genetic correlation (r_A = ?0.57 ± 0.28, P = 0.082) between the two traits (slower animals are less vigilant while foraging). We found no evidence of differential survival or longevity associated with particular phenotypes of either trait. The genetic correlation may persist because of environmental heterogeneity and genotype‐by‐environment interactions maintaining the correlation, or because there are two ways to solve the problem of foraging in exposed areas: be very vigilant and rely on early detection coupled with speed to escape, or reduce vigilance to minimize time spent in an exposed location. Both strategies seem to be equally successful, and this ‘locomotor ability‐wariness’ syndrome may therefore allow slow animals to compensate behaviourally for their impaired locomotor ability.     

Age at maturation has sex- and temperature-specific effects on telomere length in a fish

Telomeres are highly conserved nucleoprotein structures which protect genome integrity. The length of telomeres is influenced by both genetic and environmental factors, but relatively little is known about how different hereditary and environmental factors interact in determining telomere length. We manipulated growth rates and timing of maturation by exposing full-sib nine-spined sticklebacks (Pungitius pungitius) to two different temperature treatments and quantified the effects of temperature treatments, sex, timing of maturation, growth rate and family (genetic influences) on telomere length. We did not find the overall effect of temperature treatment on the relative telomere length. However, we found that variation in telomere length was related to timing of maturation in a sex- and temperature-dependent manner. Telomere length was negatively related to age at maturation in elevated temperature and early maturing males and females differed in telomere length. Variation in growth rate did not explain any variation in telomere length. The broad sense heritability (h ²) of telomere length was estimated at h ² = 0.31 ? 0.47, suggesting predominance of environmental over genetic determinants of telomere length variability. This study provides the first evidence that age at maturation together with factors associated with it are influencing telomere length in an ectotherm. Future studies are encouraged to identify the extent to which these results can be replicated in other ectotherms.     

Natural selection on the genetical component of variance in body condition in a wild bird population

Although there is substantial evidence that skeletal measures of body size are heritable in wild animal populations, it is frequently assumed that the nonskeletal component of body weight (or ‘condition’) is determined primarily by environmental factors, in particular nutritional state. We tested this assumption by quantifying the genetic and environmental components of variance in fledgling body condition index (=relative body weight) in a natural population of collared flycatchers (Ficedula albicollis), and compared the strength of natural selection on individual breeding values with that on phenotypic values. A mixed model analysis of the components of variance, based on an ‘animal model’ and using 18 years of data on 17 717 nestlings, revealed a significant additive genetic component of variance in body condition, which corresponded to a narrow sense heritability (h²) of 0.30 (SE=0.03). Nongenetic contributions to variation in body condition were large, but there was no evidence of dominance variance nor of contributions from early maternal or common environment effects (pre‐manipulation environment) in condition at fledging. Comparison of pre‐ and post‐selection samples revealed virtually identical h² of body condition index, despite the fact that there was a significant decrease (35%) in the levels of additive genetic variance from fledging to breeding. The similar h² in the two samples occurred because the environmental component of variance was also reduced by selection, suggesting that natural selection was acting on both genotypic and environmental variation. The effects of selection on genetic variance were confirmed by calculation of the selection differentials for both phenotypic values and best linear unbiased predictor (BLUP) estimates of breeding values: there was positive directional selection on condition index both at the phenotypic and the genotypic level. The significant h² of body condition index is consistent with data from human and rodent populations showing significant additive genetic variance in relative body mass and adiposity, but contrasts with the common assumption in ecology that body condition reflects an individual’s nongenetic nutritional state. Furthermore, the substantial reduction in the additive genetic component of variance in body condition index suggests that selection on environmental deviations cannot alone explain the maintenance of additive genetic variation in heritable traits, but that other mechanisms are needed to explain the moderate to high heritabilities of traits under consistent and strong directional selection.     

Evolutionary potential of thermal preference and heat tolerance in Drosophila subobscura

Evolutionary change of thermal traits (i.e., heat tolerance and behavioural thermoregulation) is one of the most important mechanisms exhibited by organisms to respond to global warming. However, the evolutionary potential of heat tolerance, estimated as narrow‐sense heritability, depends on the methodology employed. An alternative adaptive mechanism to buffer extreme temperatures is behavioural thermoregulation, although the association between heat tolerance and thermal preference is not clearly understood. We suspect that methodological effects associated with the duration of heat stress during thermal tolerance assays are responsible for missing this genetic association. To test this hypothesis, we estimated the heritabilities and genetic correlations for thermal traits in Drosophila subobscura, using high‐temperature static and slow ramping assays. We found that heritability for heat tolerance was higher in static assays (h² = 0.134) than in slow ramping assays (h² = 0.084), suggesting that fast assays may provide a more precise estimation of the genetic variation of heat tolerance. In addition, thermal preference exhibited a low heritability (h² = 0.066), suggesting a reduced evolutionary response for this trait. We also found that the different estimates of heat tolerance and thermal preference were not genetically correlated, regardless of how heat tolerance was estimated. In conclusion, our data suggest that these thermal traits can evolve independently in this species. In agreement with previous evidence, these results indicate that methodology may have an important impact on genetic estimates of heat tolerance and that fast assays are more likely to detect the genetic component of heat tolerance.     

Heritability of age at first birth in captive olive baboons

The evolution of life history traits is a topic of growing interest in primatology. Traits associated with fertility, such as age at menarche and age at first birth, have great significance for natural selection, and knowing the genetic basis of such demographic traits may improve our understanding of population dynamics. Knowledge of the heritability of reproductive traits may also have practical implications for the management of captive breeding colonies. A maximum likelihood method was used to estimate heritability of age at first birth for a sample of female olive baboons resident at the Southwest Foundation for Biomedical Research. Only animals born at the Foundation that were caged in mixed sex groups and that had previously given birth were included in the sample (n = 316). There were 117 independent individuals and 199 individuals in 35 pedigrees composed of 2 to 26 members. Age at first birth ranged from 3.85 years to 13.11 years. Age at first birth is highly heritable (h² = 0.87) with no evidence for maternal effects or a dominance genetic component. This level of genetic variability in a fitness-related trait is contrary to evolutionary expectation and may reflect the uniform environment of a captive breeding situation. Thus, the heritability observed in this population may be taken as an upper bound for that in natural populations. © 1995 Wiley-Liss, Inc.     

Heritability of sperm length in the bumblebee Bombus terrestris

Sperm length is highly variable, both between and within species, but the evolutionary significance of this variation is poorly understood. Sexual selection on sperm length requires a significant additive genetic variance, but few studies have actually measured this. Here we present the first estimates of narrow sense heritability of sperm length in a social insect, the bumblebee Bombus terrestris. In spite of a balanced and straightforward rearing design of colonies, and the possibility to replicate measurements of sperm within single males nested within colonies, the analysis proved to be complex. Several appropriate statistical models were derived, each depending on different assumptions. The heritability estimates obtained ranged from h ² = 0.197 ± 0.091 to h ² = 0.429 ± 0.154. All our estimates were substantially lower than previous estimates of sperm length heritability in non-social insects and vertebrates.     

Familial aggregation of heart rate variability based on short recordings – the kibbutzim family study

The objective of this study was to assess the familial aggregation of heart rate variability (HRV), a readily measurable noninvasive reflection of cardiac autonomic function. Familial correlations were analyzed in 451 kibbutz members aged 15–97 years belonging to 80 kindreds. Five-minute duration Holter recordings made during silent supine spontaneous breathing and metronomic breathing were analyzed in the time and frequency domains. The present analysis considers the familial correlations and the heritability estimates of two time-domain indices, the standard deviation (SD) of the R-R interval (RR), reflecting total variability, and the root mean square of successive differences in RR intervals (RMSSD), reflecting vagal (parasympathetic) tone. During free breathing, age- and sex-adjusted correlations between parents and their children (r=0.24 for both indices) and between adult siblings above 30 years of age (r=0.24 and r=0.34 for SD and RMSSD, respectively) were statistically significant, whereas spouse correlations (r=–0.04, r=–0.02 for SD and RMSSD, respectively) and correlations in younger siblings (r=–0.22 and r=0.01, respectively) were not. Significant heritability estimates were demonstrated for the two indices (h ²=0.41 for SD and h ²=0.39 for RMSSD). These findings suggest that familial aggregation of HRV characteristics is determined mostly by genetic factors and less so by environmental factors and provide a basis for continuing the investigation into the underlying genetic influences on HRV. Received: 26 August 1997 / Accepted: 15 March 1998     

SEX CHROMOSOME LINKED GENETIC VARIANCE AND THE EVOLUTION OF SEXUAL DIMORPHISM OF QUANTITATIVE TRAITS

Theory predicts that sex chromsome linkage should reduce intersexual genetic correlations thereby allowing the evolution of sexual dimorphism. Empirical evidence for sex linkage has come largely from crosses and few studies have examined how sexual dimorphism and sex linkage are related within outbred populations. Here, we use data on an array of different traits measured on over 10,000 individuals from two pedigreed populations of birds (collared flycatcher and zebra finch) to estimate the amount of sex‐linked genetic variance (h²_z). Of 17 traits examined, eight showed a nonzero h²_Z estimate but only four were significantly different from zero (wing patch size and tarsus length in collared flycatchers, wing length and beak color in zebra finches). We further tested how sexual dimorphism and the mode of selection operating on the trait relate to the proportion of sex‐linked genetic variance. Sexually selected traits did not show higher h²_Z than morphological traits and there was only a weak positive relationship between h²_Z and sexual dimorphism. However, given the relative scarcity of empirical studies, it is premature to make conclusions about the role of sex chromosome linkage in the evolution of sexual dimorphism.     

Probability of Inadmissible Estimates of Heritability from Full-Sib Analysis Under a General Model of Gene Action

Evaluation of probabilities of the heritability (h²) estimates in full-sib analysis falling outside the permissible limits [0,1] was undertaken for several combinations of sire/dam numbers, h² and proportions of dominance and additive × additive epistatic variances, assuming two full-sibs per mating and the dominance related epistasis as negligible. In the light of the results use of sire component and sire-dam combination has been recommended in the estimation of heritability of lowly and highly heritable traits respectively.     

Association between the COMT Val158Met polymorphism and breast cancer risk: a meta-analysis of 30,199 cases and 38,922 controls

Many studies have reported the role of COMT Val158Met with breast cancer risk, but the results remained controversial. In addition, previous meta-analysis on COMT Val158Met showed conflicting results. Hence, we performed a meta-analysis to investigate the association between breast cancer and COMT Val158Met (30,199 cases and 38,922 controls) in different inheritance models. When all the eligible studies were pooled into this meta-analysis, there was no evidence of significant association between breast cancer risk and COMT Val158Met polymorphism in any genetic model (dominant model: odds ratio [OR] = 0.99, 95% confidence interval [CI] = 0.94–1.04, P value of heterogeneity test [P _h] = 0.009, I ² = 36.9%; recessive model: OR = 0.97, 95% CI = 0.92–1.02, P _h = 0.044, I ² = 28.6%; additive model: OR = 0.98, 95% CI = 0.91–1.05, P _h = 0.004, I ² = 40.4%). However, significant between-study heterogeneity was detected in any genetic model. Hence, we performed the stratified analysis according to ethnicity, source of controls, menopausal status, and family history. In the stratified analysis by ethnicity significantly decreased breast cancer risk was observed in Caucasian population (recessive model: OR = 0.96, 95% CI = 0.92–1.00, P _h = 0.419, I ² = 3.1%). In conclusion, this meta-analysis indicates that COMT Val158Met polymorphism may be associated with decreased breast cancer risk in Caucasian population. However, a study with the larger sample size is needed to further evaluated gene-environment interaction on COMT Val158Met polymorphisms and breast cancer risk.     

Genetic influences on growth traits of BMI: a longitudinal study of adult twins

Objective: To investigate the interplay between genetic factors influencing baseline level and changes in BMI in adulthood. Methods and Procedures: A longitudinal twin study of the cohort of Finnish twins (N = 10,556 twin individuals) aged 20–46 years at baseline was conducted and followed up 15 years. Data on weight and height were obtained from mailed surveys in 1975, 1981, and 1990. Results: Latent growth models revealed a substantial genetic influence on BMI level at baseline in males and females (heritability (h²) 80% (95% confidence interval 0.79–0.80) for males and h² = 82% (0.81, 0.84) for females) and a moderate‐to‐high influence on rate of change in BMI (h² = 58% (0.50, 0.69) for males and h² = 64% (0.58, 0.69) for females). Only very weak evidence for genetic pleiotropy was observed; the genetic correlation between baseline and rate of change in BMI was very modest (−0.070 (–0.13, −0.068) for males and 0.04 (0.00, 0.08) for females. Discussion: Our population‐based results provide a basis for identifying genetic variants for change in BMI, in particular weight gain. Furthermore, they demonstrate for the first time that such genetic variants for change in BMI are likely to be different from those affecting level of BMI.