Maternal genetic effects set the potential for evolution in a free-living vertebrate population

Heritable maternal effects have important consequences for the evolutionary dynamics of phenotypic traits under selection, but have only rarely been tested for or quantified in evolutionary studies. Here we estimate maternal effects on early-life traits in a feral population of Soay sheep (Ovis aries) from St Kilda, Scotland. We then partition the maternal effects into genetic and environmental components to obtain the first direct estimates of maternal genetic effects in a free-living population, and furthermore test for covariance between direct and maternal genetic effects. Using an animal model approach, direct heritabilities (h2) were low but maternal genetic effects (m2) represented a relatively large proportion of the total phenotypic variance for each trait (birth weight m2=0.119, birth date m2=0.197, natal litter size m2=0.211). A negative correlation between direct and maternal genetic effects was estimated for each trait, but was only statistically significant for natal litter size (ram= -0.714). Total heritabilities (incorporating variance from heritable maternal effects and the direct-maternal genetic covariance) were significant for birth weight and birth date but not for natal litter size. Inadequately specified models greatly overestimated additive genetic variance and hence direct h2 (by a factor of up to 6.45 in the case of birth date). We conclude that failure to model heritable maternal variance can result in over- or under-estimation of the potential for traits to respond to selection, and advocate an increased effort to explicitly measure maternal genetic effects in evolutionary studies.     

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.     

Fixed and random effects in the variation of the finger ridge count: a study of fragile-X families.

A maximum-likelihood scoring technique for analysis of pedigree data allows for the concurrent estimation of random and of fixed effects in a quantitative trait. We included both types of effects in genetic models, to study the sources of variation in finger ridge count in 54 large families affected with the fragile-X disorder. The fixed effects were represented by fragile X and sex, and the random effects by environmental and genetic variance. We found a significant effect of fragile X in the mean of the finger ridge count on the thumb (finger 1) and index finger (finger 2), which had the lowest heritability and a negligible nonadditive component of genetic variance. This was in contrast with ridge counts on fingers 3 and 4, which showed little fragile-X effect, but high heritability and a significant nonadditive component. A contrast in genetic properties for ridge counts on fingers 1 and 2, compared with these counts on the remaining three fingers, may be relevant to increased selection pressures on functions of the thumb and of the index finger in evolution of modern man. We have also demonstrated an important effect of fragile X in increasing the additive variance in covariance, especially between male pairs. These findings suggest that the effect of the fragile-X genotype in finger ridge count is additive and superimposed on the normal hereditary variations in this trait.     

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.     

Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia)

The forces driving the evolution of extra-pair reproduction in socially monogamous animals remain widely debated and unresolved. One key hypothesis is that female extra-pair reproduction evolves through indirect genetic benefits, reflecting increased additive genetic value of extra-pair offspring. Such evolution requires that a female's propensity to produce offspring that are sired by an extra-pair male is heritable. However, additive genetic variance and heritability in female extra-pair paternity (EPP) rate have not been quantified, precluding accurate estimation of the force of indirect selection. Sixteen years of comprehensive paternity and pedigree data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) showed significant additive genetic variance and heritability in the proportion of a female's offspring that was sired by an extra-pair male, constituting major components of the genetic architecture required for extra-pair reproduction to evolve through indirect additive genetic benefits. However, estimated heritabilities were moderately small (0.12 and 0.18 on the observed and underlying latent scales, respectively). The force of selection on extra-pair reproduction through indirect additive genetic benefits may consequently be relatively weak. However, the additive genetic variance and non-zero heritability observed in female EPP rate allow for multiple further genetic mechanisms to drive and constrain mating system evolution.     

Ontogeny of additive and maternal genetic effects: lessons from domestic mammals

Evolution of size and growth depends on heritable variation arising from additive and maternal genetic effects. Levels of heritable (and nonheritable) variation might change over ontogeny, increasing through "variance compounding" or decreasing through "compensatory growth." We test for these processes using a meta-analysis of age-specific weight traits in domestic ungulates. Generally, mean standardized variance components decrease with age, consistent with compensatory growth. Phenotypic convergence among adult sheep occurs through decreasing environmental and maternal genetic variation. Maternal variation similarly declines in cattle. Maternal genetic effects are thus reduced with age (both in absolute and relative terms). Significant trends in heritability (decreasing in cattle, increasing in sheep) result from declining maternal and environmental components rather than from changing additive variation. There was no evidence for increasing standardized variance components. Any compounding must therefore be masked by more important compensatory processes. While extrapolation of these patterns to processes in natural population is difficult, our results highlight the inadequacy of assuming constancy in genetic parameters over ontogeny. Negative covariance between direct and maternal genetic effects was common. Negative correlations with additive and maternal genetic variances indicate that antagonistic pleiotropy (between additive and maternal genetic effects) may maintain genetic variance and limit responses to selection.     

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.     

Genetic study of the height and weight process during infancy.

Longitudinal height and weight data from 4649 Dutch twin pairs between birth and 2.5 years of age were analyzed. The data were first summarized into parameters of a polynomial of degree 4 by a mixed-effects procedure. Next, the variation and covariation in the parameters of the growth curve (size at one year of age, growth velocity, deceleration of growth, rate of change in deceleration [i.e., jerk] and rate of change in jerk [i.e., snap]) were decomposed into genetic and nongenetic sources. Additionally, the variation in the estimated size at birth and at 2 years of age interpolated from the polynomial was decomposed into genetic and nongenetic components. Variation in growth was best characterized by a genetic model which included additive genetic, common environmental and specific environmental influences, plus effects of gestational age. The effect of gestational age was largest for size at birth, explaining 39% of the variance. The differences between monozygotic and dizygotic twin correlations were largest for size at 1 and 2 years of age and growth velocity of weight, which suggests that these parameters are more influenced by heritability than size at birth, deceleration and jerk. The percentage of variance explained by additive genetic influences for height at 2 years of age was 52% for females and 58% for males. For weight at 2 years of age, heritability was approximately 58% for both sexes. Variation in snap height for males was also mainly influenced by additive genetic factors, while snap for females was influenced by both additive genetic and common environmental factors. The correlations for the additive genetic and common environmental factors for deceleration and snap are large, indicating that these parameters are almost entirely under control of the same additive genetic and common environmental factors. Female jerk and snap, and also female height at birth and height at 2 years of age, are mostly under control of the same additive genetic factor.     

Quantitative genetics of bioenergetics and growth-related traits in the wild mammal, Phyllotis darwini

We studied the potential for response to selection in typical physiological-thermoregulatory traits of mammals such as maximum metabolic rate (MMR), nonshivering thermogenesis (NST) and basal metabolic rate (BMR) on cold-acclimated animals. We used an animal model approach to estimate both narrow-sense heritabilities (h2) and genetic correlations between physiological and growth-related traits. Univariate analyses showed that MMR presented high, significant heritability (h2 = 0.69 +/- 0.35, asymptotic standard error), suggesting the potential for microevolution in this variable. However, NST and BMR presented low, nonsignificant h2, and NST showed large maternal/common environmental/nonadditive effects (c2 = 0.34 +/- 0.17). Heritabilities were large and significant (h2 > 0.5) for all growth-related traits (birth mass, growth rate, weaning mass). The only significant genetic correlations we found between a physiological trait and a growth-related trait was between NST and birth mass (r = -0.74; P < 0.05). Overall, these results suggest that additive genetic variance is present in several bioenergetic traits, and that genetic correlations could be present between those different kinds of traits.     

The genetic architecture of maternal effects across ontogeny in the red deer

Maternal effects, either environmental or genetic in origin, are an underappreciated source of phenotypic variance in natural populations. Maternal genetic effects have the potential to constrain or enhance the evolution of offspring traits depending on their magnitude and their genetic correlation with direct genetic effects. We estimated the maternal effect variance and its genetic component for 12 traits expressed over the life history in a pedigreed population of wild red deer (morphology, survival/longevity, breeding success). We only found support for maternal genetic effect variance in the two neonatal morphological traits: birth weight ( = 0.31) and birth leg length ( = 0.17). For these two traits, the genetic correlation between maternal and direct additive effects was not significantly different from zero, indicating no constraint to evolution from genetic architecture. In contrast, variance in maternal genetic effects enhanced the additive genetic variance available to respond to natural selection. Maternal effect variance was negligible for late-life traits. We found no evidence for sex differences in either the direct or maternal genetic architecture of offspring traits. Our results suggest that maternal genetic effect variance declines over the lifetime, but also that this additional heritable genetic variation may facilitate evolutionary responses of early-life traits.     

Genetic parameters of body weight in sheep estimated via random regression and multi-trait animal models

Variance components for five consecutive measurements of body weight in Polish sheep were estimated using random regression and multi-trait animal models. The data included between 7856 and 31694 body weight records at 5 age classes from birth to 150 days of age. The random additive genetic, maternal environmental and individual permanent environmental effects were fitted. All variance components were increasing over time (not at equal rates), which reflects increasing phenotypic mean and variance with age. Direct heritability tended to increase with age, whereas the effect of dam was reduced for older ages, and the proportion of permanent environmental component was relatively stable. Generally, similar tendencies were registered for estimates obtained via multi-trait animal model. The results confirm that there is a scope for genetic improvement in growth pattern in Polish sheep.     

A meta-analysis of the heritability of developmental stability

The existence of additive genetic variance in developmental stability has important implications for our understanding of morphological variation. The heritability of individual fluctuating asymmetry and other measures of developmental stability have frequently been estimated from parent-offspring regressions, sib analyses, or from selection experiments. Here we review by meta-analysis published estimates of the heritability of developmental stability, mainly the degree of individual fluctuating asymmetry in morphological characters. The overall mean effect size of heritabilities of individual fluctuating asymmetry was 0.19 from 34 studies of 17 species differing highly significantly from zero (P < 0.0001). The mean heritability for 14 species was 0.27. This indicates that there is a significant additive genetic component to developmental stability. Effect size was larger for selection experiments than for studies based on parent-offspring regression or sib analyses, implying that genetic estimates were unbiased by maternal or common environment effects. Additive genetic coefficients of variation for individual fluctuating asymmetry were considerably higher than those for character size per se. Developmental stability may be significantly heritable either because of strong directional selection, or fluctuating selection regimes which prevent populations from achieving a high degree of developmental stability to current environmental and genetic conditions.     

Twin study of the heritability of recognition thresholds for sour and salty taste

Seventy-four pairs of monozygotic (identical) twins and 35 pairs of dizygotic (fraternal) twins provided recognition thresholds (modified Harris-Kalmus test) for the sourness of citric acid and the saltiness of sodium chloride during the Twins Days Festival in Twinsburg, OH. Variance components (ACE) models were applied to the data: total variation = additive genetic (A) + common environment (C) + nonshared environment (E). The best-fit model of variation in recognition thresholds for sourness included an additive genetic factor, accounting for 53% of the variance, but no common environment component. This level of heritability, on par with that of sensitivity to the bitter compounds 6-n-propylthiouracil and phenylthiocarbamide, strongly suggests that genetic factors play a larger role than shared environment in determining individual differences in recognition thresholds for sourness. In contrast, the best-fit model for saltiness recognition included a common environment component, accounting for 22% of the variance in thresholds, but no additive component. This result suggests that environment plays a larger role than genetics in determining individual differences in recognition thresholds for saltiness.     

Quantitative genetic parameters for wild stream‐living brown trout: heritability and parental effects

Adaptability depends on the presence of additive genetic variance for important traits. Yet few estimates of additive genetic variance and heritability are available for wild populations, particularly so for fishes. Here, we estimate heritability of length‐at‐age for wild‐living brown trout (Salmo trutta), based on long‐term mark‐recapture data and pedigree reconstruction based on large‐scale genotyping at 15 microsatellite loci. We also tested for the presence of maternal and paternal effects using a Bayesian version of the Animal model. Heritability varied between 0.16 and 0.31, with reasonable narrow confidence bands, and the total phenotypic variance increased with age. When introducing dam as an additional random effect (accounting for c. 7% of total phenotypic variance), the level of additive genetic variance and heritability decreased (0.12–0.21). Parental size (both for sires and for dams) positively influenced length‐at‐age for juvenile trout – either through direct parental effects or through genotype‐environment correlations. Length‐at‐age is a complex trait reflecting the effects of a number of physiological, behavioural and ecological processes. Our data show that fitness‐related traits such as length‐at‐age can retain high levels of additive genetic variance even when total phenotypic variance is high.     

The heritability of human longevity: A population-based study of 2872 Danish twin pairs born 1870–1900

The aim of this study was to explore, in a large and non-censored twin cohort, the nature (i.e., additive versus non-additive) and magnitude (i.e., heritability) of genetic influences on inter-individual differences in human longevity. The sample comprised all identified and traced non-emigrant like-sex twin pairs born in Denmark during the period 1870–1900 with a zygosity diagnosis and both members of the pairs surviving the age of 15 years. A total of 2872 pairs were included. Age at death was obtained from the Danish Central Person Register, the Danish Cause-of-Death Register and various other registers. The sample was almost non-censored on the date of the last follow-up (May 1, 1994), all but 0.6% had died, leaving a total of 2872 pairs for analysis. Proportions of variance attributable to genetic and environmental factors were assessed from variance-covariance matrices using the structural equation model approach. The most parsimonious explanation of the data was provided by a model that included genetic dominance (non-additive genetic effects caused by interaction within gene loci) and non-shared environmental factors (environmental factors that are individual-specific and not shared in a family). The heritability of longevity was estimated to be 0.26 for males and 0.23 for females. The small sex-difference was caused by a greater impact of non-shared environmental factors in the females. Heritability was found to be constant over the three 10-year birth cohorts included. Thus, longevity seems to be only moderately heritable. The nature of genetic influences on longevity is probably non-additive and environmental influences non-shared. There is no evidence for an impact of shared (family) environment.     

Genetic parameters for growth traits of a Brazilian Bos taurus x Bos indicus beef composite

The genetic analysis of composite data is very complicated, mainly because it is necessary to adjust data to the effects of heterosis and breed complementarity, and because there is usually considerable confounding of these data with several other effects, such as contemporary group effects, breed composition of the animal and maternal breed composition, among others. Data on birth weight (n = 151,083), weaning weight adjusted to 205 days (n = 137,257), yearling weight adjusted to 390 days (n = 61,410), weight gain from weaning to yearling (n = 56,653), and scrotum circumference (n = 23,323) and muscle score (n = 54,770), both adjusted to 390 days, from Bos taurus x Bos indicus composite beef calves born from 1994 to 2003 were analyzed to estimate (co)variance components and genetic parameters of growth traits. The animals belonged to the Montana Tropical program. Estimation was made by three models that approach adjustment to heterozygosis in order to suggest the best model. The RM model included contemporary groups, class of age of dam, outcrossing percentages for direct and maternal effects, and direct and maternal additive genetic breed effects as covariates; the R model was the same as RM, but without additive maternal breed effects, and H was the same as RM, but not considering any additive breed effect. Both R2 values and consistency of genetic parameters indicate that the more complex model (RM), which considers maternal and individual additive genetic breed effect, produces the best estimates when compared to other models. The R model seems to overestimate (co)variance components. The magnitudes of direct and maternal heritability estimates, obtained in this study, would permit genetic improvement for weight and growth traits, as much by selection of direct genetic effects for weight and growth as for the improvement of maternal performance, but in different lineages. Therefore, the correlations between these effects were unfavorable.     

A genome scan for quantitative trait loci in a wild population of red deer (Cervus elaphus)

Recent empirical evidence indicates that although fitness and fitness components tend to have low heritability in natural populations, they may nonetheless have relatively large components of additive genetic variance. The molecular basis of additive genetic variation has been investigated in model organisms but never in the wild. In this article we describe an attempt to map quantitative trait loci (QTL) for birth weight (a trait positively associated with overall fitness) in an unmanipulated, wild population of red deer (Cervus elaphus). Two approaches were used: interval mapping by linear regression within half-sib families and a variance components analysis of a six-generation pedigree of >350 animals. Evidence for segregating QTL was found on three linkage groups, one of which was significant at the genome-wide suggestive linkage threshold. To our knowledge this is the first time that a QTL for any trait has been mapped in a wild mammal population. It is hoped that this study will stimulate further investigations of the genetic architecture of fitness traits in the wild.     

Inheritance of size and shape in a natural population of collared flycatchers,Ficedula albicollis

Four external skeletal and three feather dimensions were measured on adult collared flycatchers (Ficedula albicollis) and their adult offspring. By using mid-offspring-midparent regressions, all traits were found to be heritable with an arithmetic mean heritability of 0.46. Heritability estimates from full-sib analyses were about 1.5 times higher (mean 0.67), indicating that variation in traits was affected by shared nest environment among full-sibs. The overall body size as measured by principal component one (PC1) was found to be heritable (h² = 0.40). However, this multivariate measure of heritability was not significant in offspring-father comparison, while highly so in offspring-mother comparison (h² = 0.60). Low offspring-father resemblance was evident also in univariate estimates of heritability. Possible causes of this (extra-pair copulations, maternal effects, sex-linked variance) are discussed. Genetic correlations among seven traits were estimated to be low (mean 0.22), and of similar magnitude or higher than phenotypic correlations (mean 0.18). All genetic correlations were positive. Genetic and phenotypic correlations as well as covariances were fairly similar to each other (r = 0.85 and r = 0.87, respectively). Environmental correlations did not follow the pattern of genetic correlations (r = 0.11), but were more similar to phenotypic correlations (r = 0.60). Given the low genetic correlations and moderate heritabilities, the overall conclusion is that the external morphology of collared flycatchers is largely under additive genetic control and that there is a strong potential for evolutionary change in morphology even under complex multivariate selection.     

Phenotypic plasticity for life-history traits in Drosophila melanogaster. III. Effect of the environment on genetic parameters.

We estimated genetic and environmental variance components for developmental time and dry weight at eclosion in Drosophila melanogaster raised in ten different environments (all combinations of 22, 25 and 28 degrees C and 0.5, 1 and 4% yeast concentration, and 0.25% yeast at 25 degrees C). We used six homozygous lines derived from a natural population for complete diallel crosses in each environment. Additive genetic variances were consistently low for both traits (h2 around 10%). The additive genetic variance of developmental time was larger at lower yeast concentrations, but the heritability did not increase because other components were also larger. The additive genetic effects of the six parental lines changed ranks across environments, suggesting a mechanism for the maintenance of genetic variation in heterogenous environments. The variance due to non-directional dominance was small in most environments. However, there was directional dominance in the form of inbreeding depression for both traits. It was pronounced at high yeast levels and temperatures but disappeared when yeast or temperature were decreased. This meant that the heterozygous flies were more sensitive to environmental differences than homozygous flies. Because dominance effects are not heritable, this suggests that the evolution of plasticity can be constrained when dominance effects are important as a mechanism for plasticity.     

Heritability of short-scale natal dispersal in a large-scale foraging bird, the wandering albatross

Natal dispersal is a key life history trait for the evolution and adaptation of wild populations. Although its evolution has repeatedly been related to the social and environmental context faced by individuals, parent-offspring regressions have also highlighted a possible heritable component. In this study, we explore heritability of natal dispersal, at the scale of the sub-Antarctic Possession Island, for a large-scale foraging seabird, the Wandering albatross Diomedea exulans, exploiting a pedigree spanning over four decades and a maximum of four generations. The comparison of three different methods shows that heritability on the liability scale can vary drastically depending on the type of model (heritability from 6% to 86%), with a notable underestimation by restricted maximum likelihood animal models (6%) compared to Bayesian animal models (36%). In all cases, however, our results point to significant additive genetic variance in the individual propensity to disperse, after controlling for substantial effects of sex and natal colony. These results reveal promising evolutionary potential for short-scale natal dispersal, which could play a critical role for the long-term persistence of this species on the long run.