Levels Of Additive Genetic Variance Research Articles

Revisiting Heritable Variation and Limits to Species Distribution: Recent Developments

There are several evolutionary reasons why species distributions are locally and geographically limited, and these mostly revolve around gene flow and levels of genetic variation in populations. While there has been progress in developing models assessing the impact of gene flow, empirical data on hypotheses about factors limiting distributions remain rare. A few recent plant studies have highlighted that levels of additive genetic variance are not limiting, suggesting a role for gene flow. However, some animal studies, mostly onDrosophilaspecies, have refocused attention on heritable variation as an evolutionary reason for distribution limits. There is a need for comparative studies that examine levels of heritable variation across related species groups with broad and narrow distributions, and also across a range of traits including those likely to be under selection at borders. These studies will help to test specific predictions about the relative importance of genetic variance and gene flow in limiting current borders and also help in predicting the impact of future environmental changes on distribution shifts.

Repeatability of cell-mediated and innate immunity, and other fitness-related traits, in the Grey Partridge

Immunocompetence is considered a reliable indicator of general body condition and ultimately of fitness. It has been suggested that, as a parameter subjected to intense directional selection, the level of additive genetic variance expressed should be reduced; on the other hand, theoretical models of host–parasite coevolution assume that variation in parasite resistance has a genetic basis. Contradictory results have been reported in birds, since the heritability of immune responses varies from nil to high. In this study of Grey Partridge (Perdix perdix (L., 1758)), we examined the heritability of immune condition (PHA reaction, an index of T-cell-mediated immunocompetence) and of some parameters traditionally considered important for chick survival, such as egg mass and chick growth. Two statistical approaches were used: parent–offspring regression and full-sibling intra-clutch repeatability. The repeatability of other parameters that reflect egg quality (egg proteins, lipids, and carotenoids) and of substances that confer innate immunity (lysozyme and avidin) was also investigated. In agreement with previous studies, we found nonsignificant heritability for cell-mediated immunocompetence. In contrast, there were significant repeatabilities of chick mass and several egg characteristics (mass, size, total proteins), while lipid and carotenoid concentrations were not repeatable. For the first time in birds, we found significant repeatability of two molecules, lysozyme and avidin, that confer innate immunity to the developing embryo.

VERY LOW ADDITIVE GENETIC VARIANCE AND EVOLUTIONARY POTENTIAL IN MULTIPLE POPULATIONS OF TWO RAINFOREST DROSOPHILA SPECIES

Most quantitative traits are thought to exhibit high levels of genetic variance and evolutionary potential. However, this conclusion may be biased by a lack of studies on nonmodel organisms and may not generalize to restricted species. A recent study on a single, southern population of the rainforest-restricted Drosophila birchii failed to find significant additive genetic variance for the desiccation resistance trait; however, it is unclear whether this pattern extends to other D. birchii populations or to other rainforest species. Here we use an animal model design to show very low levels of additive genetic variance for desiccation resistance in multiple populations of two highly sensitive rainforest species of Drosophila from tropical northeastern Australia. In contrast, relatively high levels of genetic variance were found for morphological traits in all populations of the species tested. This indicates limited evolutionary potential for evolving increased desiccation resistance in these rainforest restricted species.

Natural selection on floral traits of female Silene dioica by a sexually transmitted disease

Floral traits endowing high reproductive fitness can also affect the probability of plants contracting sexually transmitted diseases. We explore how variations in floral traits influence the fitness of Silene dioica females in their interactions with pollinators carrying pollen or spores of the sterilizing anther-smut fungus Microbotryum violaceum. We collected healthy and infected plants in a highly diseased population and grew them under conditions that 'cure' infected individuals, and used standard regression methods to detect natural selection on floral traits. Narrow-sense heritabilities, coefficients of additive genetic variation (CV(A)) and genetic correlations among traits were estimated from paternal half-sib groups. Pollinator preferences imposed strong direct and directional selection on traits affecting female attractiveness and pollen-/spore-capturing abilities. Levels of additive genetic variance were high in these traits, suggesting that rapid responses to selection are possible. By considering our results in the light of spatial and temporal heterogeneity resulting from the colonization dynamics typical for this species, we suggest that the conflicting selective effects of pollen/spore loads lead to the maintenance of genetic variation in these traits.

The evolution of male genitalia: patterns of genetic variation and covariation in the genital sclerites of the dung beetle Onthophagus taurus

Three main hypotheses, have been invoked to explain divergent genital evolution, the lock and key, pleiotropy, and sexual selection hypotheses, each of which make different predictions about how genital traits are inherited. Here we used a half-sib breeding design to examine the patterns of genetic variation and covariation between male genital sclerites, and their covariance with general body morphology in the dung beetle Onthophagus taurus. We found CV(A)'s and CV(P)'s were similar for both genital and general morphological traits and that CV(R)'s were large for both trait types. We found that male genital sclerites were negatively genetically correlated with general morphological traits. Variation in male genital morphology has direct implications for a male's fertilization success and the resulting sexual selection acting on male genitalia is predicted to maintain high levels of additive genetic variance. Contrary to this prediction, we found that individual genital sclerites all had low levels of additive genetic variance and large maternal and environmental sources of variation. Our data suggest that the genital sclerites in O. taurus are not inherited independently but as a genetically integrated unit. More importantly, the way the different sclerites function to influence male fertilization success reflects this genetic integration. Even though levels of V(A) in individual genital sclerites may be low, there may still be sufficient V(A) in multivariate trait space for selection to generate evolutionary change in the overall morphology of male genitalia.

Genetic analysis of female reproduction traits of farmed coho salmon (Oncorhyncus kisutch)

Based on 8 years of data on 891 daughters from 190 sires and 398 dams, females produced an average (standard deviation) of 4251 (957) green eggs with a total weight of about 680 (191) g; the females produced 3226 (1255) eyed eggs, average egg weight was 180 (27) mg, and the average day of spawning was 137.5 (9.8) days measured from December 31. Average body weight was 3247 (879) g at harvest, 3702 (876) g at spawning and 3022 (730) g post-spawning. Estimated heritability of weight of green eggs spawned was 0.39, while that for number of green eggs was 0.42, that for heritability for average egg weight (egg size) and number of eyed eggs were slightly lower at 0.32 and 0.33, respectively, while the estimate for spawn day was low (0.24). Number of green eggs was highly, and positively, correlated with weight of eggs spawned (0.79), number of eyed eggs (0.82) and number of eyed eggs with weight of eggs spawned (0.53) and spawn day (0.52). The genetic correlations between number of eggs and average egg weight were negative (−0.63 for green eggs and −0.44 for eyed eggs). None of the estimated genetic correlations between spawn day and the four measures of fish size differed from zero, suggesting genetic independence of spawning date and body size, within spawning season; however, this may have been due to the inclusion of only early spawning females in the study. Estimates of genetic correlations between the various measures of fish size were all positive and ranged from 0.60 to 0.70 for spawning weight and spawning length, spawning length and post-spawning weight and harvest weight and post-spawning length of females. Spawning weight was highly correlated with weight of eggs spawned (0.69) and moderately related genetically to number of green eggs (0.34) and average weight of ova (0.37). Estimates of genetic correlation between spawning weight and number of eyed eggs did not differ from zero. The corresponding phenotypic correlations all were low or near zero. Harvest weight and post-spawning weight were not correlated with number of green or eyed eggs, but were associated with egg weight and weight of eggs spawned; both genetic correlations were 0.46 for harvest weight, while the correlations with post-spawning weight were 0.37 for egg weight and 0.56 for weight of eggs spawned. The results indicate that the coho population under study contains a high level of additive genetic variation for all traits related to female reproduction and estimates of genetic correlations suggest that correlated changes that may accompany selection for larger body size at market will be favourable in most instances.

Evolvability and genetic constraint in Dalechampia blossoms: genetic correlations and conditional evolvability.

The short-term evolvability of a character is closely related to its level of additive genetic variation. However, a large component of the variation in any one character may be pleiotropically linked to other characters under the influence of different selective factors. Therefore, the organization of the organism into quasi-independent modules may be an important prerequisite for evolvability. In this paper we propose to study character evolvability in terms of conditional genetic variation. By estimating the amount of genetic variation in a character, y, that is independent of other characters, x, we can assess the evolvability of y when there is stabilizing selection on x. We suggest that systematic use of conditioning may help build a picture of modular organization and quasi-independent evolvability. As an illustration, we use this approach to assess the evolvability of floral characters in Dalechampia scandens (Euphorbiaceae). Although our study population had relatively low levels of genetic variation at the outset, we find evidence that conditioning may lead to substantial further reduction in the genetic variation available for independent adaptation. This provides additional evidence that the D. scandens blossom is constrained in its short-term evolvability.

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.

Fluctuating environments and the role of mutation in maintaining quantitative genetic variation.

We study a class of genetic models in which a quantitative trait determined by several additive loci is subject to temporally fluctuating selection. Selection on the trait is assumed to be stabilizing but with an optimum that varies periodically and might be perturbed stochastically. The population mates at random, is infinitely large and has discrete generations. We pursue a statistical and numerical approach, covering a wide range of ecological and genetic parameters, to determine the potential of fluctuating environments to maintain quantitative genetic variation. Whereas, in contrast to some recent claims, this potential seems to be rather limited in the absence of recurrent mutation, fluctuating environments might, in combination with it, often generate high levels of additive genetic variation. We investigate how the genetic variation maintained depends on the ecological parameters and on the underlying genetics.

The genetics of maternal care: direct and indirect genetic effects on phenotype in the dung beetle Onthophagus taurus.

While theoretical models of the evolution of parental care are based on the assumption of underlying genetic variance, surprisingly few quantitative genetic studies of this life-history trait exist. Estimation of the degree of genetic variance in parental care is important because it can be a significant source of maternal effects, which, if genetically based, represent indirect genetic effects. A major prediction of indirect genetic effect theory is that traits without heritable variation can evolve because of the heritable environmental variation that indirect genetic effects provide. In the dung beetle, Onthophagus taurus, females provide care to offspring by provisioning a brood mass. The size of the brood mass has pronounced effects on offspring phenotype. Using a half-sib breeding design we show that the weight of the brood mass females produce exhibits significant levels of additive genetic variance due to sires. However, variance caused by dams is considerably larger, demonstrating that maternal effects are also important. Body size exhibited low additive genetic variance. However, body size exerts a strong maternal influence on the weight of brood masses produced, accounting for 22% of the nongenetic variance in offspring body size. Maternal body size also influenced the number of offspring produced but there was no genetic variance for this trait. Offspring body size and brood mass weight exhibited positive genetic and phenotypic correlations. We conclude that both indirect genetic effects, via maternal care, and nongenetic maternal effects, via female size, play important roles in the evolution of phenotype in this species.

Experimental and demographic analyses of growth rate and sexual size dimorphism in a lizard, Sceloporus undulatus

Sexual size dimorphism (SSD) is a common phenomenon caused by a variety of environmental and genetic mechanisms in animals. In the current study, we investigate the demography of a population of eastern fence lizards (Sceloporus undulatus) to compare age structure and survivorship between the sexes, and we examine growth rates of juveniles under both natural and controlled laboratory conditions to elucidate causes of SSD in this species. Furthermore, using our laboratory growth data, we examine the heritability of juvenile growth rates. Our results show that SSD develops in the field before the end of the first year of age (before sexual maturity) because juvenile females grow more rapidly than juvenile males. In the laboratory environment, however, we observed no sexual difference in growth rates for lizards up to the size of maturity in the field. Thus, sexual differences in growth rate and subsequent development of SSD in this population are highly plastic and subject to strong proximal control. We found high levels of additive genetic variance for juvenile growth, indicating a strong potential for selection to operate on juvenile growth rates. Our results indicate that selection on juvenile growth rate could account for differences in growth among populations but would not necessarily contribute to SSD within our population due to the high plasticity in growth rate.

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

Abstract 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.

Positive genetic correlation between parasite resistance and body size in a free-living ungulate population.

Parasite resistance and body size are subject to directional natural selection in a population of feral Soay sheep (Ovis aries) on the island of St. Kilda, Scotland. Classical evolutionary theory predicts that directional selection should erode additive genetic variation and favor the maintenance of alleles that have negative pleiotropic effects on other traits associated with fitness. Contrary to these predictions, in this study we show that there is considerable additive genetic variation for both parasite resistance, measured as fecal egg count (FEC), and body size, measured as weight and hindleg length, and that there are positive genetic correlations between parasite resistance and body size in both sexes. Body size traits had higher heritabilities than parasite resistance. This was not due to low levels of additive genetic variation for parasite resistance, but was a consequence of high levels of residual variance in FEC. Measured as coefficients of variation, levels of additive genetic variation for FEC were actually higher than for weight or hindleg length. High levels of additive genetic variation for parasite resistance may be maintained by a number of mechanisms including high mutational input, balancing selection, antagonistic pleiotropy, and host-parasite coevolution. The positive genetic correlation between parasite resistance and body size, a trait also subject to sexual selection in males, suggests that parasite resistance and growth are not traded off in Soay sheep, but rather that genetically resistant individuals also experience superior growth.

Individual variation in growth trajectories: phenotypic and genetic correlations in ontogeny of the house finch (Carpodacus mexicanus)

Abstract We studied patterns of growth in a recently established natural population of the house finch (Carpodacus mexicanus) to examine whether phenotypic and genetic covariation among age-specific trait values is likely to constrain morphological change favoured by selection acting on adults. We found variable patterns of allometric relationships during ontogeny, and documented relatively weak covariations among ages or among traits in individual growth trajectories. Frequent compensatory growth largely cancelled out the initial differences among nestlings, potentially enabling house finches to raise offspring under diverse and unpredictable environmental conditions. Moderate levels of additive genetic variance in morphological traits throughout ontogeny, and relatively low and fluctuating phenotypic and genetic covariation among ages imply strong potential for evolutionary change in morphological traits under selection. This conclusion is consistent with the profound population-level divergence in morphological patterns that accompanied very successful colonization of most of North America by the house finch over the last 50 years.

Lifetime Reproductive Success and Heritability in Nature.

The observation that traits closely related to fitness ("fitness traits") have lower heritabilities than traits more distantly associated with fitness has traditionally been framed in terms of Fisher's fundamental theorem of natural selection-fitness traits are expected to have low levels of additive genetic variance due to rapid fixation of alleles conferring highest fitness. Subsequent treatments have challenged this view by pointing out that high environmental and nonadditive genetic contributions to phenotypic variation may also explain the low heritability of fitness traits. Analysis of a large data set from the collared flycatcher Ficedula albicollis confirmed a previous finding that traits closely associated with fitness tend to have lower heritability. However, analysis of coefficients of additive genetic variation (CVA) revealed that traits closely associated with fitness had higher levels of additive genetic variation (VA) than traits more distantly associated with fitness. Hence, the negative relationship between a trait's association with fitness and its heritability was not due to lower levels of VA in fitness traits but was due to their higher residual variance. However, whether the high residual variance was mainly due to higher levels of environmental variance or due to higher levels of nonadditive genetic variance remains a challenge to be addressed by further studies. Our results are consistent with earlier suggestions that fitness-related traits may have more complex genetic architecture than traits more distantly associated with fitness.

Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas.

Comparative studies of the genetic architecture of different types of traits were initially prompted by the expectation that traits under strong directional selection (fitness traits) should have lower levels of genetic variability than those mainly under weak stabilizing selection (nonfitness traits). Hence, early comparative studies revealing lower heritabilities of fitness than nonfitness traits were first framed in terms of giving empirical support for this prediction, but subsequent treatments have effectively reversed this view. Fitness traits seem to have higher levels of additive genetic variance than nonfitness traits - an observation that has been explained in terms of the larger number loci influencing fitness as compared to nonfitness traits. This hypothesis about the larger functional architecture of fitness than nonfitness traits is supported by their higher mutational variability, which is hard to reconcile without evoking capture of mutational variability over many loci. The lower heritabilities of fitness than nonfitness traits, despite the higher additive genetic variance of the former, occur because of their higher residual variances. Recent comparative studies of dominance contributions for different types of traits, together with theoretical predictions and a large body of indirect evidence, suggest an important role of dominance variance in determining levels of residual variance for fitness-traits. The role of epistasis should not be discounted either, since a large number of loci increases the potential for epistatic interactions, and epistasis is strongly implicated in hybrid breakdown.

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

Abstract 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).

Heritability of size but not symmetry in a sexually selected trait chosen by female earwigs

The heritability of fitness-related traits remains an area of contention in evolutionary biology: despite theoretical arguments for little additive genetic variance in fitness-related traits, significant heritabilities in secondary sexual traits are an increasingly reported phenomenon. Some evidence suggests that fluctuating asymmetry (FA) in secondary sexual traits may reflect the genetic quality of the trait bearer. Consequently, females in search of ‘good genes’ should pay attention to ornament symmetry. If FA does reflect genetic quality which females can assess, an additive genetic component would be expected. Using sib analysis, we found that the length of the sexually selected forceps of male European earwigs (Forficula auricularia) have significant levels of additive genetic variance. However, using both sib analysis and an estimate derived from the genetic and phenotypic correlations of the left and right sides, we found no evidence for additive genetic variance in forceps FA. These results thus provide evidence that female preferences for exaggerated secondary sexual traits can influence trait expression in offspring.

CHANGES IN THE HERITABILITY OF FIVE MORPHOLOGICAL TRAITS UNDER COMBINED ENVIRONMENTAL STRESSES IN DROSOPHILA MELANOGASTER.

Heritabilities and evolvabilities for morphological traits were compared between two environments in Drosophila melanogaster using parent-offspring comparisons. One of the environments was favorable. The other stressful environment involved a combination of repeated cold shocks, poor nutrition, and ethanol added to the medium, which markedly decreased viability. For wing traits, heritabilities were relatively lower in the stressful environment, while heritabilities for bristle traits were not influenced by conditions. Heritability changes were largely due to an increase in the environmental variance under stress, whereas levels of additive genetic variance were relatively constant. Evolvabilities were similar between environments except for crossvein length.

HERITABILITIES OF DOMINANCE-RELATED TRAITS IN MALE BANK VOLES (CLETHRIONOMYS GLAREOLUS).

A number of studies have shown that in several animal species females prefer dominant males as mating partners, but fewer attempts have been made to measure possible indirect benefits of this choice. One reason for this may be that, even though dominance is a widely used concept, the definition of dominance still remains controversial Furthermore, defining and measuring the heritability of social behaviors is problematic because they are not individual traits but, by definition, involve interactions between at least two individuals. In this study we estimated heritabilities and coefficients of additive genetic variances (CVA ) for male traits that are closely associated with dominance and female mating preferences in bank voles (Clethrionomys glareolus). The heritability values were estimated using father-offspring regression. All heritability estimates were relatively high ranging from 0.531 (urine marking) to 0.767 (preputial glands). The CVA -values indicated high levels of additive genetic variance especially in the characters most closely related to dominance: the weight of preputial glands and urine marking behavior. All phenotypic correlations among the traits measured were significantly positive and the genetic correlations were of similar magnitude as the corresponding phenotypic counterparts. Even though heritabilities may be lower in the natural environment than under controlled laboratory conditions, our results suggest that characters closely related to dominance may be at least partly genetically determined.