Ontogenetic patterns in heritable variation for body size: using random regression models in a wild ungulate population

Body size is an important determinant of fitness in many organisms. While size will typically change over the lifetime of an individual, heritable components of phenotypic variance may also show ontogenetic variation. We estimated genetic (additive and maternal) and environmental covariance structures for a size trait (June weight) measured over the first 5 years of life in a natural population of bighorn sheep Ovis canadensis. We also assessed the utility of random regression models for estimating these structures. Additive genetic variance was found for June weight, with heritability increasing over ontogeny because of declining environmental variance. This pattern, mirrored at the phenotypic level, likely reflects viability selection acting on early size traits. Maternal genetic effects were significant at ages 0 and 1, having important evolutionary implications for early weight, but declined with age being negligible by age 2. Strong positive genetic correlations between age-specific traits suggest that selection on June weight at any age will likely induce positively correlated responses across ontogeny. Random regression modeling yielded similar results to traditional methods. However, by facilitating more efficient data use where phenotypic sampling is incomplete, random regression should allow better estimation of genetic (co)variances for size and growth traits in natural populations.     

Where do all the maternal effects go? Variation in offspring body size through ontogeny in the live-bearing fish Poecilia parae

Maternal effects are an important source of adaptive variation, but little is known about how they vary throughout ontogeny. We estimate the contribution of maternal effects, sire genetic and environmental variation to offspring body size from birth until 1 year of age in the live-bearing fish Poecilia parae. In both the sexes, maternal effects on body size were initially high in juveniles, and then declined to zero at sexual maturity. In sons, this was accompanied by a sharp rise in sire genetic variance, consistent with the expression of Y-linked loci affecting male size. In daughters, all variance components decreased with time, consistent with compensatory growth. There were significant negative among-dam correlations between early body size and the timing of sexual maturity in both sons and daughters. However, there was no relationship between early life maternal effects and adult longevity, suggesting that maternal effects, although important early in life, may not always influence late life-history traits.     

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.     

A general definition of the heritable variation that determines the potential of a population to respond to selection

Genetic selection is a major force shaping life on earth. In classical genetic theory, response to selection is the product of the strength of selection and the additive genetic variance in a trait. The additive genetic variance reflects a population's intrinsic potential to respond to selection. The ordinary additive genetic variance, however, ignores the social organization of life. With social interactions among individuals, individual trait values may depend on genes in others, a phenomenon known as indirect genetic effects. Models accounting for indirect genetic effects, however, lack a general definition of heritable variation. Here I propose a general definition of the heritable variation that determines the potential of a population to respond to selection. This generalizes the concept of heritable variance to any inheritance model and level of organization. The result shows that heritable variance determining potential response to selection is the variance among individuals in the heritable quantity that determines the population mean trait value, rather than the usual additive genetic component of phenotypic variance. It follows, therefore, that heritable variance may exceed phenotypic variance among individuals, which is impossible in classical theory. This work also provides a measure of the utilization of heritable variation for response to selection and integrates two well-known models of maternal genetic effects. The result shows that relatedness between the focal individual and the individuals affecting its fitness is a key determinant of the utilization of heritable variance for response to selection.     

A mother’s legacy: the strength of maternal effects in animal populations

Although mothers influence the traits of their offspring in many ways beyond the transmission of genes, it remains unclear how important such ‘maternal effects’ are to phenotypic differences among individuals. Synthesizing estimates derived from detailed pedigrees, we evaluated the amount of phenotypic variation determined by maternal effects in animal populations. Maternal effects account for half as much phenotypic variation within populations as do additive genetic effects. Maternal effects most greatly affect morphology and phenology but, surprisingly, are not stronger in species with prolonged maternal care than in species without. While maternal effects influence juvenile traits more than adult traits on average, they do not decline across ontogeny for behaviour or physiology, and they do not weaken across the life cycle in species without maternal care. These findings underscore maternal effects as an important source of phenotypic variation and emphasise their potential to affect many ecological and evolutionary processes.     

Developmental Quantitative Genetics, Conditional Epigenetic Variability and Growth in Mice

Ontogenetic variation in the causal components of phenotypic variability and covariability is described for body weight and tail length in mice derived from a full 7 X 7 diallel cross. Age-related changes in additive, dominance, sex-linked and maternal variance and covariance between 14 and 70 days of age are described. Age-specific variance components at time t are conditioned on the causal genetic effects at time (t - 1). This procedure demonstrates the generation of significant episodes of new genetic variation arising at specific intervals during ontogeny. These episodes of new genetic variation are placed in the context of epigenetic models in developmental quantitative genetics. These results are also concordant on recent findings on age-specific gene expression in mouse growth as shown by QTL analyses.     

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.     

Sexual selection in the cricket <Emphasis Type="Italic">Gryllus bimaculatus</Emphasis>: no good genes?

Recent studies have suggested that females of the field cricket Gryllus bimaculatus exercise post-copulatory choice over the paternity of their offspring. There is evidence that these choices are made in relation to the genetic compatibility of mates rather than their absolute quality, but the magnitude of heritable differences in males has not been thoroughly examined. Using a half-sib breeding design we measured additive genetic variance and dam effects in a suite of reproductive and non-reproductive traits. Both components explained relatively little of the phenotypic variance across traits. The dam component in our design contains variance caused by both maternal effects and dominance. If maternal effects are negligible as suggested by previous studies, our data suggest that dominance variance is an important source of variation in these traits. The lack of additive genetic variation, but possible existence of large amounts of non-additive genetic variation is consistent with the idea that female mate choice and multiple mating may be driven by differences in genetic compatibility between potential mates rather than by differences in genetic quality.     

Sexual selection in the cricket <Emphasis Type="Italic">Gryllus bimaculatus</Emphasis>: no good genes?

Recent studies have suggested that females of the field cricket Gryllus bimaculatus exercise post-copulatory choice over the paternity of their offspring. There is evidence that these choices are made in relation to the genetic compatibility of mates rather than their absolute quality, but the magnitude of heritable differences in males has not been thoroughly examined. Using a half-sib breeding design we measured additive genetic variance and dam effects in a suite of reproductive and non-reproductive traits. Both components explained relatively little of the phenotypic variance across traits. The dam component in our design contains variance caused by both maternal effects and dominance. If maternal effects are negligible as suggested by previous studies, our data suggest that dominance variance is an important source of variation in these traits. The lack of additive genetic variation, but possible existence of large amounts of non-additive genetic variation is consistent with the idea that female mate choice and multiple mating may be driven by differences in genetic compatibility between potential mates rather than by differences in genetic quality.     

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.     

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.     

(Co)Variance components and genetic parameter estimates for growth traits in Moghani sheep

Genetic parameters were estimated for birth weight (BW), weaning weight (WW), yearling weight (YW), average daily gain from birth to weaning (ADG1) and average daily gain from weaning to yearling (ADG2) in Moghani sheep. Maximum number of data was 4237 at birth, but only 1389 records at yearling were investigated. The data was collected from 1995 to 2007 at the Breeding Station of Moghani sheep in Jafarabad, Moghan, Iran. (Co)Variance components and genetic parameters were estimated with different models which including direct effects, with and without maternal additive genetic effects as well as maternal permanent environmental effects using restricted maximum likelihood (REML) method. The most appropriate model for each trait was determined based on likelihood ratio tests and Akaike's Information Criterion (AIC). Maternal effects were important only for pre-weaning traits. Direct heritability estimates for BW, ADG1, WW, ADG2 and YW were 0.07, 0.08, 0.09, 0.09 and 0.17, respectively. Fractions of variance due to maternal permanent environmental effects on phenotypic variance were 0.08 for ADG1. Maternal heritability estimates for BW and WW were 0.18 and 0.06, respectively. Multivariate analysis was performed using the most appropriate models obtained in univariate analysis. Direct genetic correlations among studied traits were positive and ranged from 0.37 for BW–ADG2 to 0.85 for ADG1–YW. Maternal genetic correlation estimate between BW and WW was 0.33. Phenotypic and environmental correlation estimates were generally lower than those of genetic correlation. Low direct heritability estimates imply that mass selection for these traits results in slow genetic gain.     

Estimating variance components and heritabilities in the wild: a case study using the ‘animal model’ approach

Using a genealogy containing over 1800 dams and nearly 400 sires (estimated by genetic paternity techniques), combined with maximum likelihood procedures and an ‘animal model’, we have estimated the heritabilities, genetic correlations and variance components of three morphometric traits in the Soay sheep (Ovis aries) on St Kilda, Scotland. This approach allows heritabilities to be estimated in natural populations that violate the assumptions of offspring–parent regression methods. Maternal (or paternal) effects can also be estimated under natural conditions. We demonstrate that all the traits, body weight, hind leg length and incisor arcade breadth, have low but significant heritabilities. Body weight, the trait that experiences the strongest selection, had the lowest heritability but the highest additive genetic coefficient of variation. An evolutionary response to selection is predicted. When maternal effects were not taken into consideration heritabilities were over‐estimated, although this effect was only significant in female offspring.     

Genetic and maternal effect influences on viability of common frog tadpoles under different environmental conditions

The influence of environmental stress on the expression of genetic and maternal effects on the viability traits has seldom been assessed in wild vertebrates. We have estimated genetic and maternal effects on the viability (viz probability of survival, probability of being deformed, and body size and shape) of common frog, Rana temporaria, tadpoles under stressful (low pH) and nonstressful (neutral pH) environmental conditions. A Bayesian analysis using generalized linear mixed models was applied to data from a factorial laboratory experiment. The expression of additive genetic variance was independent of pH treatments, and all traits were significantly heritable (survival: h2 approximately 0.08; deformities: h2 approximately 0.26; body size: h2 approximately 0.12; body shape: h2 approximately 0.14). Likewise, nonadditive genetic contributions to variation in all traits were significant, independent of pH treatments and typically of magnitude similar to the additive genetic effects. Maternal effects were large for all traits, especially for viability itself, and their expression was partly dependent on the environment. In the case of body size, the maternal effects were mediated largely through egg size. In general, the results give little evidence for the conjecture that environmental stress created by low pH would impact strongly on the genetic architecture of fitness-related traits in frogs, and hamper adaptation to stress caused by acidification. The low heritabilities and high dominance contributions conform to the pattern typical for traits subject to relatively strong directional selection.     

Parental effects on embryonic viability and growth in Arctic charr Salvelinus alpinus at two incubation temperatures

The parental influences on three progeny traits (survival to eyed‐embryo stage, post‐hatching body length and yolk‐sac volume) of Arctic charr Salvelinus alpinus were studied under two thermal conditions (2 and 7° C) using a factorial mating design. The higher temperature resulted in elevated mortality rates and less advanced development at hatching. Survival was mostly attributable to maternal effects at both temperatures, but the variation among families was dependent on egg size only at the low temperature. No additive genetic variation (or pure sire effect) could be observed, whereas the non‐additive genetic effects (parental combination) contributed to offspring viability at 2° C. In contrast, any observable genetic variance in survival was lost at 7° C, most likely due to the increased environmental variance. Irrespective of temperature, dam and sire–dam interaction contributed significantly to the phenotypic variation in both larval length and yolk size. A significant proportion of the variation in larval length was also due to the sire effect at 2° C. Maternal effects were mediated partly through egg size, but as a whole, they decreased in importance at the high temperature, enabling a concomitant increase in non‐additive genetic effects. For larval length, however, the additive component, like maternal effects, decreased at 7° C. The present results suggest that an exposure to thermal stress during incubation can modify the genetic architecture of early developmental traits in S. alpinus and presumably constrain their short‐term adaptive potential and evolvability by increasing the amount of environmentally induced variation.     

Local Adaptation and Genetics of Acid-Stress Tolerance in the Moor Frog, Rana arvalis

As potential to adapt to environmental stress can be essential for population persistence, knowledge on the genetic architecture of local adaptation is important for conservation genetics. We investigated the relative importance of additive genetic, dominance and maternal effects contributions to acid stress tolerance in two moor frog (Rana arvalis) populations originating from low and neutral pH habitats. Experiments with crosses obtained from artificial matings revealed that embryos from the acid origin population were more tolerant to low pH than embryos from the neutral origin population in embryonic survival rates, but not in terms of developmental stability, developmental and growth rates. Strong maternal effect and small additive genetic contributions to variation were detected in all traits in both populations. In general, dominance contributions to variance in different traits were of similar magnitude to the additive genetic effects, but dominance effects outweighed the additive genetic and maternal effects contributions to early growth in both populations. Furthermore, the expression of additive genetic variance was independent of pH treatment, suggesting little additive genetic variation in acid stress tolerance. The results suggest that although local genetic adaptation to acid stress has taken place, the current variation in acid stress tolerance in acidified populations may owe largely to non-genetic effects. However, low but significant heritabilities (h ² 0.07–0.22) in all traits – including viability itself – under a wide range of pH conditions suggests that environmental stress created by low pH is unlikely to lower moor frog populations' ability to respond to selection in the traits studied. Nevertheless, acid conditions could lower populations' ability to respond to selection in the long run through reduction in effective population size.     

Responses of alloplasmic (cytoplasm=Triticum timopheevii) and euplasmic wheats (Triticum aestivum) to photoperiod and vernalization

Summary Heritability estimated from sire family variance components, ignoring dams, pools conventional paternal and maternal half sib estimates, in a way which is biased upward, and sub-optimal for minimizing the sampling variance. Standard error of a sire family estimate will be smaller than that of the equivalent paternal half sib estimate, but not as small as that of an estimate obtained by optimal pooling of paternal and maternal half sib estimates. If only additive genetic variance components are significant, the bias may be removed by use of a computed average genetic relationship for sire families, in place of a nominal R = 0.25. Average genetic relationship may be computed from mean and variance of dam family size within sire families. If dominance, epistatic, or maternal components are significant, this simple correction is not appropriate. In situations likely to be encountered in large domestic species such as sheep and cattle (dam family size small and uniform) bias will be negligible. The method could be useful where cost of dam identification is a limiting factor.     

Evolution of Adaptation and Mate Choice: Parental Relatedness Affects Expression of Phenotypic Variance in a Natural Population

Mating between relatives generally results in reduced offspring viability or quality, suggesting that selection should favor behaviors that minimize inbreeding. However, in natural populations where searching is costly or variation among potential mates is limited, inbreeding is often common and may have important consequences for both offspring fitness and phenotypic variation. In particular, offspring morphological variation often increases with greater parental relatedness, yet the source of this variation, and thus its evolutionary significance, are poorly understood. One proposed explanation is that inbreeding influences a developing organism’s sensitivity to its environment and therefore the increased phenotypic variation observed in inbred progeny is due to greater inputs from environmental and maternal sources. Alternatively, changes in phenotypic variation with inbreeding may be due to additive genetic effects alone when heterozygotes are phenotypically intermediate to homozygotes, or effects of inbreeding depression on condition, which can itself affect sensitivity to environmental variation. Here we examine the effect of parental relatedness (as inferred from neutral genetic markers) on heritable and nonheritable components of developmental variation in a wild bird population in which mate choice is often constrained, thereby leading to inbreeding. We found greater morphological variation and distinct contributions of variance components in offspring from highly related parents: inbred offspring tended to have greater environmental and lesser additive genetic variance compared to outbred progeny. The magnitude of this difference was greatest in late-maturing traits, implicating the accumulation of environmental variation as the underlying mechanism. Further, parental relatedness influenced the effect of an important maternal trait (egg size) on offspring development. These results support the hypothesis that inbreeding leads to greater sensitivity of development to environmental variation and maternal effects, suggesting that the evolutionary response to selection will depend strongly on mate choice patterns and population structure.     

Quantitative genetic and translocation experiments reveal genotype‐by‐environment effects on juvenile life‐history traits in two populations of Chinook salmon (Oncorhynchus tshawytscha)

Understanding the genetic architecture of phenotypic plasticity is required to assess how populations might respond to heterogeneous or changing environments. Although several studies have examined population‐level patterns in environmental heterogeneity and plasticity, few studies have examined individual‐level variation in plasticity. Here, we use the North Carolina II breeding design and translocation experiments between two populations of Chinook salmon to detail the genetic architecture and plasticity of offspring survival and growth. We followed the survival of 50 800 offspring through the larval stage and used parentage analysis to examine survival and growth through freshwater rearing. In one population, we found that additive genetic, nonadditive genetic and maternal effects explained 25%, 34% and 55% of the variance in larvae survival, respectively. In the second population, these effects explained 0%, 24% and 61% of the variance in larvae survival. In contrast, fry survival was regulated primarily by additive genetic effects, which indicates a shift from maternal to genetic effects as development proceeds. Fry growth also showed strong additive genetic effects. Translocations between populations revealed that offspring survival and growth varied between environments, the degree of which differed among families. These results indicate genetic differences among individuals in their degree of plasticity and consequently their ability to respond to environmental variation.     

Quantitative genetics of growth and development time in the burying beetle Nicrophorus pustulatus in the presence and absence of post-hatching parental care

Despite a growing interest in the evolutionary aspects of maternal effects, few studies have examined the genetic consequences of maternal effects associated with parental care. To begin to provide data on nonlaboratory or nondomestic animals, we compared the effect of presence and absence of parental care on phenotype expression of larval mass and development time at different life-history stages in the burying beetle Nicrophorus pustulatus. This beetle has facultative care; parents can feed their larvae through regurgitation of digested carrion or offspring can feed by themselves from previously prepared carrion. To investigate larval responses to these two levels of care, including estimates of additive genetic effects, maternal effects, and genotype-by-environment interactions, we used a half-sibling split-family breeding experiment-raising half of the offspring of a family in the presence of their mother and the other half without their mother present. Larvae reared with their mother present were on average heavier and developed faster, although some of the differences in development decreased or were eliminated by the adult stage. These results suggest that presence or absence of post-hatching maternal care plays an important role in phenotype expression early in life, whereas later the phenotype of the offspring is determined mainly by the genotype and/or unshared environmental effects. Our study also permitted us to examine the differences in genetic effects between the two care environments. Heritabilities, maternal/common environment effect, and most genetic correlations did not differ between the care treatments. Genetic analyses revealed substantial additive genetic effects for development time but small effects for measures of body mass. Maternal plus common environment effects were high for measures of mass but low for development time, suggesting that indirect genetic effects of maternal and/or common environment are less important for the evolution of development time than for mass. Estimates of genetic correlations revealed a trade-off between the duration of the two development stages after the offspring left the carrion. There was also a negative genetic correlation between the time spent on carrion and the mass at 72 h, when mothers usually stop feeding. The analysis of genotype-by-environment interactions indicates substantial variation among maternal families in response to care. Presence or absence of parental care may therefore contribute to the additive genetic variance through its interaction with the maternal component of the additive genetic variance. The presence of this interaction further suggests that parents may vary in care strategies, with some parents dispersing after preparation of the carrion and some parents staying with the larvae. This interaction may help maintain genetic variation in growth, development time, and parental care behavior. Additional work is needed, however, to quantify indirect genetic effects and genetic variation in parental care behavior itself.