HERITABILITY OF FITNESS COMPONENTS IN A WILD BIRD POPULATION

Consistently with the prediction that selection should deplete additive genetic variance ( V_A ) in fitness, traits closely associated to fitness have been shown to exhibit low heritabilities ( h ²= V_A /( V_A + V_R )). However, empirical data from the wild indicate that this is in fact due to increased residual variance ( V_R ), rather than due to decreased additive genetic variance, but the studies in this topic are still rare. We investigated relationships between trait heritabilities, additive genetic variances, and traits' contribution to lifetime reproductive success (≈fitness) in a red-billed gull ( Larus novaehollandiae ) population making use of animal model analyses as applied to 15 female and 13 male traits. We found that the traits closely associated with fitness tended to have lower heritabilities than traits less closely associated with fitness. However, in contrast with the results of earlier studies in the wild, the low heritability of the fitness-related traits was not only due to their high residual variance, but also due to their low additive genetic variance. Permanent environment effects—integrating environmental effects experienced in early life as well as nonadditive genetic effects—on many traits were large, but unrelated to traits' importance for fitness.     

ON THE LOW HERITABILITY OF LIFE-HISTORY TRAITS

Life-history traits such as longevity and fecundity often show low heritability. This is usually interpreted in terms of Fisher's fundamental theorem to mean that populations are near evolutionary equilibrium and genetic variance in total fitness is low. We develop the causal relationship between metric traits and life-history traits to show that a life-history trait is expected to have a low heritability whether or not the population is at equilibrium. This is because it is subject to all the environmental variation in the metric traits that affect it plus additional environmental variation. There is no simple prediction regarding levels of additive genetic variance in life-history traits, which may be high at equilibrium. Several other patterns in the inheritance of life-history traits are readily predicted from the causal model. These include the strength of genetic correlations between life-history traits, levels of nonadditive genetic variance, and the inevitability of genotype-environment interaction.     

Components of variance underlying fitness in a natural population of the great tit Parus major

Traits that are closely associated with fitness tend to have lower heritabilities (h2) than those that are not. This has been interpreted as evidence that natural selection tends to deplete genetic variation more rapidly for traits more closely associated with fitness (a corollary of Fisher's fundamental theorem), but Price and Schluter (1991) suggested the pattern might be due to higher residual variance in traits more closely related to fitness. The relationship between 10 different traits for females, seven traits for males, and overall fitness (lifetime recruitment) was quantified for great tits (Parus major) studied in their natural environment of Wytham Wood, England, using data collected over 39 years. Heritabilities and the coefficients of additive genetic and residual variance (CVA and CVR, respectively) were estimated using an "animal model." For both males and females, a trait's correlation (r) with fitness was negatively related to its h2 but positively related to its CVR. The CVA was not related to the trait's correlation with fitness in either sex. This is the third study using directly measured fitness in a wild population to show the important role of residual variation in determining the pattern of lower heritabilities for traits more closely related to fitness.     

Selection and genetic (co)variance in bighorn sheep

Genetic theory predicts that directional selection should deplete additive genetic variance for traits closely related to fitness, and may favor the maintenance of alleles with antagonistically pleiotropic effects on fitness-related traits. Trait heritability is therefore expected to decline with the degree of association with fitness, and some genetic correlations between selected traits are expected to be negative. Here we demonstrate a negative relationship between trait heritability and association with lifetime reproductive success in a wild population of bighorn sheep (Ovis canadensis) at Ram Mountain, Alberta, Canada. Lower heritability for fitness-related traits, however, was not wholly a consequence of declining genetic variance, because those traits showed high levels of residual variance. Genetic correlations estimated between pairs of traits with significant heritability were positive. Principal component analyses suggest that positive relationships between morphometric traits constitute the main axis of genetic variation. Trade-offs in the form of negative genetic or phenotypic correlations among the traits we have measured do not appear to constrain the potential for evolution in this population.     

Comparing Evolvability and Variability of Quantitative Traits

There are two distinct reasons for making comparisons of genetic variation for quantitative characters. The first is to compare evolvabilities, or ability to respond to selection, and the second is to make inferences about the forces that maintain genetic variability. Measures of variation that are standardized by the trait mean, such as the additive genetic coefficient of variation, are appropriate for both purposes. Variation has usually been compared as narrow sense heritabilities, but this is almost always an inappropriate comparative measure of evolvability and variability. Coefficients of variation were calculated from 842 estimates of trait means, variances and heritabilities in the literature. Traits closely related to fitness have higher additive genetic and nongenetic variability by the coefficient of variation criterion than characters under weak selection. This is the reverse of the accepted conclusion based on comparisons of heritability. The low heritability of fitness components is best explained by their high residual variation. The high additive genetic and residual variability of fitness traits might be explained by the great number of genetic and environmental events they are affected by, or by a lack of stabilizing selection to reduce their phenotypic variance. Over one-third of the quantitative genetics papers reviewed did not report trait means or variances. Researchers should always report these statistics, so that measures of variation appropriate to a variety of situations may be calculated.     

Lack of nonadditive genetic effects on early fecundity in Drosophila melanogaster

Fecundity is usually considered as a trait closely connected to fitness and is expected to exhibit substantial nonadditive genetic variation and inbreeding depression. However, two independent experiments, using populations of different geographical origin, indicate that early fecundity in Drosophila melanogaster behaves as a typical additive trait of low heritability. The first experiment involved artificial selection in inbred and non-inbred lines, all of them started from a common base population previously maintained in the laboratory for about 35 generations. The realized heritability estimate was 0.151 +/- 0.075 and the inbreeding depression was very small and nonsignificant (0.09 +/- 0.09% of the non-inbred mean per 1% increase in inbreeding coefficient). With inbreeding, the observed decrease in the within-line additive genetic variance and the corresponding increase of the between-line variance were very close to their expected values for pure additive gene action. This result is at odds with previous studies showing inbreeding depression and, therefore, directional dominance for the same trait and species. All experiments, however, used laboratory populations, and it is possible that the original genetic architecture of the trait in nature was subsequently altered by the joint action of random drift and adaptation to captivity. Thus, we carried out a second experiment, involving inbreeding without artificial selection in a population recently collected from the wild. In this case we obtained, again, a maximum-likelihood heritability estimate of 0.210 +/- 0.027 and very little nonsignificant inbreeding depression (0.06 +/- 0.12%). The results suggest that, for fitness-component traits, low levels of additive genetic variance are not necessarily associated with large inbreeding depression or high levels of nonadditive genetic variance.     

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 parameters related to environmental variability of weight traits in a selection experiment for weight gain in mice; signs of correlated canalised response

Data from an experimental mice population selected from 18 generations to increase weight gain were used to estimate the genetic parameters associated with environmental variability. The analysis involved three traits: weight at 21 days, weight at 42 days and weight gain between 21 and 42 days. A dataset of 5273 records for males was studied. Data were analysed using Bayesian procedures by comparing the Deviance Information Criterion (DIC) value of two different models: one assuming homogeneous environmental variances and another assuming them as heterogeneous. The model assuming heterogeneity was better in all cases and also showed higher additive genetic variances and lower common environmental variances. The heterogeneity of residual variance was associated with systematic and additive genetic effects thus making reduction by selection possible. Genetic correlations between the additive genetic effects on mean and environmental variance of the traits analysed were always negative, ranging from -0.19 to -0.38. An increase in the heritability of the traits was found when considering the genetic determination of the environmental variability. A suggested correlated canalised response was found in terms of coefficient of variation but it could be insufficient to compensate for the scale effect associated with an increase of the mean.     

Heritability and evolvability of fitness and nonfitness traits: Lessons from livestock

Data from natural populations have suggested a disconnection between trait heritability (variance standardized additive genetic variance, V_A) and evolvability (mean standardized V_A) and emphasized the importance of environmental variation as a determinant of trait heritability but not evolvability. However, these inferences are based on heterogeneous and often small datasets across species from different environments. We surveyed the relationship between evolvability and heritability in >100 traits in farmed cattle, taking advantage of large sample sizes and consistent genetic approaches. Heritability and evolvability estimates were positively correlated (r = 0.37/0.54 on untransformed/log scales) reflecting a substantial impact of V_A on both measures. Furthermore, heritabilities and residual variances were uncorrelated. The differences between this and previously described patterns may reflect lower environmental variation experienced in farmed systems, but also low and heterogeneous quality of data from natural populations. Similar to studies on wild populations, heritabilities for life‐history and behavioral traits were lower than for other traits. Traits having extremely low heritabilities and evolvabilities (17% of the studied traits) were almost exclusively life‐history or behavioral traits, suggesting that evolutionary constraints stemming from lack of genetic variability are likely to be most common for classical “fitness” (cf. life‐history) rather than for “nonfitness” (cf. morphological) traits.     

How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva

Rapid larval growth in insects may be selected for by rapid ephemeral phenological changes in food resources modifying the structure of phenotypic and genetic (co)variation in and among individual traits. We studied the relative effects of three processes which can modify expression of additive genetic and nongenetic variation in traits. First, natural selection tends to erode genetic variation in fitness-related traits. Second, there may be high variance even in traits closely coupled with fitness, if these traits are themselves products of variable lower level traits. Third, traits may be canalized by developmental processes which reduce phenotypic variation. Moreover, we investigated the phenotypic and genetic role played by the underlying traits in attaining simultaneously both large size and short development time. We measured phenotypic and genetic (co)variation in several pre- and post-ingestive foraging traits, growth, development rate, development time and size, together forming a hierarchical network of traits, in the larvae of a flush feeding geometrid, Epirrita autumnata. Rapid larval growth rate and high pupal mass are closely related to fitness in E. autumnata. Traits closely associated with larval growth displayed low levels of additive genetic variation, indicating that genetic variability may have been exhausted by selection for rapid growth. The body size of E. autumnata, in spite of its close correlation with fitness, exhibited a significant additive genetic variation, possiblye because caterpillar size is the outcome of many underlying heritable traits. The low level traits in the hierarchical net, number (indicating larval movements) and size of feeding bouts in leaves, relative consumption rate and efficiency of conversion of ingested food, displayed high levels of residual variation. High residual variation in consumption and physiological ability to handle leaf material resulted from their flexibility which reduced variation in growth rate, i.e. growth rate was canalized. We did not detect a trade-off between development time and final size. On the contrary, large pupal masses were attained by short larval periods, and this relationship was strongly genetically determined, suggesting that both developmental time and final size are expressions of the same developmental process (vigorous growth) and the same genes (or linkage disequilibrium).     

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

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

How does selfing affect the genetic variance of quantitative traits? An updated meta‐analysis on empirical results in angiosperm species

Most theoretical works predict that selfing should reduce the level of additive genetic variance available for quantitative traits within natural populations. Despite a growing number of quantitative genetic studies undertaken during the last two decades, this prediction is still not well supported empirically. To resolve this issue and confirm or reject theoretical predictions, we reviewed quantitative trait heritability estimates from natural plant populations with different rates of self‐fertilization and carried out a meta‐analysis. In accordance with models of polygenic traits under stabilizing selection, we found that the fraction of additive genetic variance is negatively correlated with the selfing rate. Although the mating system explains a moderate fraction of the variance, the mean reduction of narrow‐sense heritability values between strictly allogamous and predominantly selfing populations is strong, around 60%. Because some nonadditive components of genetic variance become selectable under inbreeding, we determine whether self‐fertilization affects the relative contribution of these components to genetic variance by comparing narrow‐sense heritability estimates from outcrossing populations with broad‐sense heritability estimated in autogamous populations. Results suggest that these nonadditive components of variance may restore some genetic variance in predominantly selfing populations; it remains, however, uncertain how these nonadditive components will contribute to adaptation.     

THE EVOLUTIONARY GENETICS OF MALE LIFE-HISTORY CHARACTERS IN DROSOPHILA MELANOGASTER

Alternative models of the maintenance of genetic variability, theories of life-history evolution, and theories of sexual selection and mate choice can be tested by measuring additive and nonadditive genetic variances of components of fitness. A quantitative genetic breeding design was used to produce estimates of genetic variances for male life-history traits in Drosophila melanogaster. Additive genetic covariances and correlations between traits were also estimated. Flies from a large, outbred, laboratory population were assayed for age-specific competitive mating ability, age-specific survivorship, body mass, and fertility. Variance-component analysis then allowed the decomposition of phenotypic variation into components associated with additive genetic, nonadditive genetic, and environmental variability. A comparison of dominance and additive components of genetic variation provides little support for an important role for balancing selection in maintaining genetic variance in this suite of traits. The results provide support for the mutation-accumulation theory, but not the antagonistic-pleiotropy theory of senescence. No evidence is found for the positive genetic correlations between mating success and offspring quality or quantity that are predicted by “good genes” models of sexual selection. Additive genetic coefficients of variation for life-history characters are larger than those for body weight. Finally, this set of male life-history characters exhibits a very low correspondence between estimates of genetic and phenotypic correlations.     

GENETIC AND ENVIRONMENTAL VARIATION IN LIFE-HISTORY TRAITS OF A MONOCARPIC PERENNIAL: A DECADE-LONG FIELD EXPERIMENT

Directional and stabilizing selection tend to deplete additive genetic variance. On the other hand, genetic variance in traits related to fitness could be retained through polygenic mutation, spatially varying selection, genotype-environment interaction, or antagonistic pleiotropy. Most estimates of genetic variance in fitness-related traits have come from laboratory studies, with few estimates of heritability made under natural conditions, particularly for longer lived organisms. Here I estimated additive genetic variance in life-history characters of a monocarpic herb, Ipomopsis aggregata, that lives for up to a decade. Experimental crosses yielded 229 full-sibships nested within 32 paternal half-sibships. More than 5000 offspring were planted as seeds into natural field sites and were followed in most cases through their entire life cycle. Survival showed substantial additive genetic variance (genetic coefficient of variation ≈ 54%). Small differences at seedling emergence were magnified over time, such that the genetic variability in survival was only detectable by tracking the success of offspring for several years starting from seed. In contrast to survival, reproductive traits such as flower number, seeds per flower, and age at flowering showed little or no genetic variability. Despite relatively high levels of additive genetic variation for some life-history characters, high environmental variance in survival resulted in very low heritabilities (0–9%) for all of these characters. Maternal effects were evident in seed mass and remained strong throughout the lengthy vegetative period. No negative genetic correlations between major components of female fitness were detected. Mean corolla width for a paternal family was, however, negatively correlated with the finite rate of increase based on female fitness. That negative correlation could help to maintain additive genetic variance in the face of strong selection through male function for wide corollas.     

Sex differences in the genetic architecture of aggressiveness in a sexually dimorphic spider

Sex differences in the genetic architecture of behavioral traits can offer critical insight into the processes of sex‐specific selection and sexual conflict dynamics. Here, we assess genetic variances and cross‐sex genetic correlations of two personality traits, aggression and activity, in a sexually size‐dimorphic spider, Nuctenea umbratica. Using a quantitative genetic approach, we show that both traits are heritable. Males have higher heritability estimates for aggressiveness compared to females, whereas the coefficient of additive genetic variation and evolvability did not differ between the sexes. Furthermore, we found sex differences in the coefficient of residual variance in aggressiveness with females exhibiting higher estimates. In contrast, the quantitative genetic estimates for activity suggest no significant differentiation between males and females. We interpret these results with caution as the estimates of additive genetic variances may be inflated by nonadditive genetic effects. The mean cross‐sex genetic correlations for aggression and activity were 0.5 and 0.6, respectively. Nonetheless, credible intervals of both estimates were broad, implying high uncertainty for these estimates. Future work using larger sample sizes would be needed to draw firmer conclusions on how sexual selection shapes sex differences in the genetic architecture of behavioral traits.     

EPISTASIS AND THE EFFECT OF FOUNDER EVENTS ON THE ADDITIVE GENETIC VARIANCE

Models of founder events have focused on the reduction in the genetic variation following a founder event. However, recent work (Bryant et al., 1986; Goodnight, 1987) suggests that when there is epistatic genetic variance in a population, the total genetic variance within demes may actually increase following a founder event. Since the additive genetic variance is a statistical property of a population and can change with the level of inbreeding, some of the epistatic genetic variance may be converted to additive genetic variance during a founder event. The model presented here demonstrates that some of the additive-by-additive epistatic genetic variance is converted to additive genetic variance following a founder event. Furthermore, the amount of epistasis converted to additive genetic variance is a function of the recombination rate and the propagule size. For a single founder event of two individuals, as much as 75% of the epistatic variance in the ancestral population may become additive genetic variance following the founder event. For founder events involving two individuals with free recombination, the relative contribution of epistasis to the additive genetic variance following a founder event is equal to its proportion of the total genetic variance prior to the founder event. Traits closely related to fitness are expected to have relatively little additive genetic variance but may have substantial nonadditive genetic variance. Founder events may be important in the evolution of fitness traits, not because they lead to a reduction in the genetic variance, but rather because they lead to an increase in the additive genetic variance.     

QUANTITATIVE GENETICS OF FITNESS TRAITS IN A WILD POPULATION OF PHLOX

To determine if the evolution of fitness traits in the annual plant, Phlox drummondii, is constrained by lack of genetic variation, we calculated the heritability and genetic correlation of 16 traits in a field population. Full- and half-sib families of seeds were generated in the greenhouse and planted back into the study population. Of 855 seeds that germinated, 609 survived to produce fruit. For each plant we measured several aspects of plant size and three components of female fecundity: total number of fruits produced, number of seeds per fruit, and mass of individual seeds. Heritability of traits ranged from 0.00 to 0.15. Several traits showed significant levels of additive genetic variance, but we found no evidence of additive genetic variance in components of female fecundity and no evidence of negative genetic correlation between fitness traits. These results suggest that evolution in this population would be constrained by lack of heritable variation in fitness traits.     

Selection,structure and the heritability of behaviour

Characters which are closely linked to fitness often have low heritabilities (V_A/V_P). Low heritabilities could be because of low additive genetic variation (V_A), that had been depleted by directional selection. Alternatively, low heritabilities may be caused by large residual variation (V_R=V_P – V_A) compounded at a disproportionately higher rate than V_A across integrated characters. Both hypotheses assume that each component of quantitative variation has an independent effect on heritability. However, V_A and V_R may also covary, in which case differences in heritability cannot be fully explained by the independent effects of elimination‐selection or compounded residual variation. We compared the central tendency of published behavioural heritabilities (mean=0.31, median=0.23) with morphological and life history data collected by 26 ). Average behavioural heritability was not significantly different from average life history heritability, but both were smaller than average morphological heritability. We cross‐classified behavioural traits to test whether variation in heritability was related to selection (dominance, domestic/wild) or variance compounding (integration level). There was a significant three‐way interaction between indices of selection and variance compounding, related to the absence of either effect at the highest integration level. At lower integration levels, high dominance variance indicated effects of selection. It was also indicated by the low CV_A of domestic species. At the same time CV_R increased disproportionately faster than CV_A across integration levels, demonstrating variance compounding. However, neither CV_R nor CV_A had a predominant effect on heritability. The partial regression coefficients of CV_R and CV_A on heritability were similar and a path analysis indicated that their (positive) correlation was also necessary to explain variation in heritability. These results suggest that relationships between additive genetic and residual components of quantitative genetic variation can constrain their independent direct effects on behavioural heritability.