QUANTITATIVE GENETICS OF SIZE AND PHENOLOGY OF LIFE-HISTORY TRAITS IN CHAMAECRISTA FASCICULATA

Despite numerous adaptive scenarios concerning the evolution of plant life-history phenologies few studies have examined the heritable basis for and genetic correlations among these phenologies. Documentation of genetic variation for and covariation among reproductive phenologies is important because it is this variation/covariation that will determine the potential for response to evolutionary forces. To address this problem, I conducted a breeding experiment to determine narrow-sense heritabilities for and genetic correlations among the phenologies of life-history events and plant size in Chamaecristafasciculata, a temperate summer annual plant species. Paternal families showed no evidence of heritable variation for two estimates of plant size, six measures of reproductive phenology or two fitness components. Similarly, paternal estimates of genetic correlations among these traits were low or zero. In contrast, maternal estimates of heritability suggested the influence of maternal parent on one estimate of plant size and four phenological traits. Likewise, maternal effects influenced maternal estimates of genetic correlations. These maternal effects can arise from three sources: endosperm nuclear, cytoplasmic genetic and/or maternal phenotypic. The degree to which the phenology of one life-history trait acts as a constraint on the evolution of other phenological traits depends on the source of the maternal influence in this species.     

On the evolution of clonal plant life histories

Clonal plant life histories are special in at least four respects: (1) Clonal plants can also reproduce vegetatively, (2) vegetative reproduction can be realised with short or long spacers, (3) and it may allow to plastically place vegetative offspring in benign patches. (4) Moreover, ramets of clonal plants may remain physically and physiologically integrated. Because of the apparent utility of such traits and because ecological patterns of distribution of clonal and non-clonal plants differ, adaptation is a tempting explanation of observed clonal life-history variation. However, adaptive evolution requires (1) heritable genetic variation and (2) a trait effect on fitness, and (3) it may be constrained if other evolutionary forces are overriding selection or by constraints, costs and trade-offs. (1) The few studies undertaken so far reported broad-sense heritability for clonal traits. Variation in selectively neutral genetic markers appears as pronounced in populations of clonal as non-clonal plants. However, neutral markers may not reflect heritable variation of life-history traits. Moreover, clonal plants may have been sampled at larger spatial scales. Empirical information on the contribution of somatic mutations to heritable variation is lacking. (2) Clonal life-history traits were found to affect fitness. However, much of this evidence stems from artificial rather than natural environments. (3) The relative importance of gene flow, inbreeding, and genetic drift, compared with selection, in the evolution of clonal life histories is hardly explored. Benefits of clonal life-history traits were frequently studied and found. However, there is also evidence for constraints, trade-offs, and costs. In conclusion, though it is very likely, that clonal life-history traits are adaptive, it is neither clear to which degree this is the case, nor which clonal life-history traits constitute adaptations to which environmental factors. Moreover, evolutionary interactions among clonal life-history traits and between clonal and non-clonal ones, such as the mating system, are not well explored. There remains much interesting work to be done in this field – which will be particularly interesting if it is done in the field.     

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.     

Covariation of larval gene expression and adult body size in natural populations of Drosophila melanogaster

Understanding adaptive phenotypic variation is one of the most fundamental problems in evolutionary biology. Genes involved in adaptation are most likely those that affect traits most intimately connected to fitness: life-history traits. The genetics of quantitative trait variation (including life histories) is still poorly understood, but several studies suggest that (1) quantitative variation might be the result of variation in gene expression, rather than protein evolution, and (2) natural variation in gene expression underlies adaptation. The next step in studying the genetics of adaptive phenotypic variation is therefore an analysis of naturally occuring covariation of global gene expression and a life-history trait. Here, we report a microarray study addressing the covariation in larval gene expression and adult body weight, a life-history trait involved in adaptation. Natural populations of Drosophila melanogaster show adaptive geographic variation in adult body size, with larger animals at higher latitudes. Conditions during larval development also affect adult size with larger flies emerging at lower temperatures. We found statistically significant differences in normalized larval gene expression between geographic populations at one temperature (genetic variation) and within geographic populations between temperatures (developmental plasticity). Moreover, larval gene expression correlated highly with adult weight, explaining 81% of its natural variation. Of the genes that show a correlation of gene expression with adult weight, most are involved in cell growth or cell maintenance or are associated with growth pathways.     

Artificial selection reveals heritable variation for developmental instability

Fluctuating (nondirectional) asymmetry (FA) of bilaterally paired structures on a symmetrical organism is commonly used to assay the developmental instability (DI) caused by environmental or genetic factors. Although evidence for natural selection to reduce FA has been reported, evidence that FA (and by extension DI) is heritable is weak. We report the use of artificial selection to demonstrate heritable variation in the fluctuating asymmetry of interlandmark distances within the wing in an outbred population of Drosophila melanogaster. Our estimates for the heritability of FA range from 0% to 1% and result in estimates for the heritability of DI as large as 20%, comparable to values typical for life-history traits. These values indicate the existence of evolutionarily relevant genetic variation for DI and the effectiveness of selection for reduced FA suggests that natural selection has not fixed all the genetic variants that would improve developmental stability in these populations.     

Experimental life-history evolution: selection on the allocation to sexual reproduction and its plasticity in a clonal plant

Abstract.— Allocation to sexual reproduction is an important life-history trait in clonal plants. Different selection pressures between competitive and competition-free environments are likely to result in the evolution of specialized genotypes and to maintain genetic variation in reproductive allocation. Moreover, selection may also result in the evolution of plastic allocation strategies. The necessary prerequisite for evolution, heritable genetic variation, can best be studied with selection experiments. Starting from a base population of 102 replicated genotypes of the clonal herb Ranunculus reptans , we imposed selection on the proportion of flowering rosettes in the absence of competition (base population: mean = 0.391, broad-sense heritability = 0.307). We also selected on the plasticity in this trait in response to competition with a naturally coexisting grass in a parallel experiment (base population: 14% lower mean in the presence of competition, broad-sense heritability = 0.072). After two generations of bidirectional selection, the proportion of flowering rosettes was 26% higher in the high line than in the low line (realized heritability ± SE = 0.205 ± 0.017). Moreover, genotypes of the high line had 11% fewer carpels per flower, a 22% lower proportion of rooted rosettes, and a 39% smaller average distance between rosettes within a clone. In the second experiment, we found no significant responses to selection for high and low plasticity in the proportion of flowering rosettes (realized heritability ± SE =–0.002 ± 0.013). Our study indicates a high heritability and potential for further evolution of the proportion of flowering rosettes in R. reptans , but not for its plasticity, which may have been fixed by past evolution at its current level. Moreover, our results demonstrate strong genetic correlations between allocation to sexual reproduction and other clonal life-history characteristics.     

Community heritability measures the evolutionary consequences of indirect genetic effects on community structure

The evolutionary analysis of community organization is considered a major frontier in biology. Nevertheless, current explanations for community structure exclude the effects of genes and selection at levels above the individual. Here, we demonstrate a genetic basis for community structure, arising from the fitness consequences of genetic interactions among species (i.e., interspecific indirect genetic effects or IIGEs). Using simulated and natural communities of arthropods inhabiting North American cottonwoods (Populus), we show that when species comprising ecological communities are summarized using a multivariate statistical method, nonmetric multidimensional scaling (NMDS), the resulting univariate scores can be analyzed using standard techniques for estimating the heritability of quantitative traits. Our estimates of the broad-sense heritability of arthropod communities on known genotypes of cottonwood trees in common gardens explained 56-63% of the total variation in community phenotype. To justify and help interpret our empirical approach, we modeled synthetic communities in which the number, intensity, and fitness consequences of the genetic interactions among species comprising the community were explicitly known. Results from the model suggest that our empirical estimates of broad-sense community heritability arise from heritable variation in a host tree trait and the fitness consequences of IGEs that extend from tree trait to arthropods. When arthropod traits are heritable, interspecific IGEs cause species interactions to change, and community evolution occurs. Our results have implications for establishing the genetic foundations of communities and ecosystems.     

Genetic Variation Underlying Sexual Behavior and Reproduction

Selection depletes additive genetic variation underlying traitsimportant in fitness. Intense mating competition and femalechoice may result in negligible heritability in males. Femalesoften appear to choose mates, however, suggesting genetic variationin males which is important to females. Evidence is reviewedon allelic substitutions, karyotypic variation, and especiallythe heritable variation of continuous traits involved in sexualbehavior and reproduction. Phenotypic variation in male matingspeed and courtship intensity, female mating and ovipositionbehavior, egg size and number, body size, parthenogenesis, andthe sex ratio generally have heritable variation. The maintenanceof genetic variation, and the meaning of heritability estimatesfor natural populations is considered.     

Individual covariation in life-history traits: seeing the trees despite the forest

We investigated the influence of age on survival and breeding rates in a long-lived species Rissa tridactyla using models with individual random effects permitting variation and covariation in fitness components among individuals. Differences in survival or breeding probabilities among individuals are substantial, and there was positive covariation between survival and breeding probability; birds that were more likely to survive were also more likely to breed, given that they survived. The pattern of age-related variation in these rates detected at the individual level differed from that observed at the population level. Our results provided confirmation of what has been suggested by other investigators: within-cohort phenotypic selection can mask senescence. Although this phenomenon has been extensively studied in humans and captive animals, conclusive evidence of the discrepancy between population-level and individual-level patterns of age-related variation in life-history traits is extremely rare in wild animal populations. Evolutionary studies of the influence of age on life-history traits should use approaches differentiating population level from the genuine influence of age: only the latter is relevant to theories of life-history evolution. The development of models permitting access to individual variation in fitness is a promising advance for the study of senescence and evolutionary processes.     

Divergent selection on,but no genetic conflict over,female and male timing and rate of reproduction in a human population

The sexes often have different phenotypic optima for important life-history traits, and because of a largely shared genome this can lead to a conflict over trait expression. In mammals, the obligate costs of reproduction are higher for females, making reproductive timing and rate especially liable to conflict between the sexes. While studies from wild vertebrates support such sexual conflict, it remains unexplored in humans. We used a pedigreed human population from preindustrial Finland to estimate sexual conflict over age at first and last reproduction, reproductive lifespan and reproductive rate. We found that the phenotypic selection gradients differed between the sexes. We next established significant heritabilities in both sexes for all traits. All traits, except reproductive rate, showed strongly positive intersexual genetic correlations and were strongly genetically correlated with fitness in both sexes. Moreover, the genetic correlations with fitness were almost identical in men and women. For reproductive rate, the intersexual correlation and the correlation with fitness were weaker but again similar between the sexes. Thus, in this population, an apparent sexual conflict at the phenotypic level did not reflect an underlying genetic conflict over the studied reproductive traits. These findings emphasize the need for incorporating genetic perspectives into studies of human life-history evolution.     

ENVIRONMENT-DEPENDENCE OF QUANTITATIVE GENETIC PARAMETERS IN IMPATIENS PALLIDA

Population response to selection depends on the presence of additive genetic variance for traits under selection. When a population enters an alien environment, environment-induced changes in the expression of genetic variance may occur. These could have large effects on the response to selection. To investigate the environment-dependence of genetic variance, we conducted a reciprocal transplant experiment between two ecotypically differentiated populations of Impatiens pallida using the progeny of a standard mating design. The floodplain site was characterized by high water availability, moderate temperatures, and continuous dense stands of Impatiens. The hillside site was drier, with larger temperature extremes and supported only scattered patches of Impatiens with significantly lower seed production and earlier mortality. Estimates of heritability were low for each of the 13 traits measured in each population and site (range from 0–28%). Additive genetic variance for life-history traits tended to be larger than for morphological traits, but genetic variance in fitness was estimated to be not significantly different from zero in all cases. Significant heritability was detected in both populations for one trait (date of first cleistogamous flower) known to be closely related to fitness on the hillside. In general, heritability was reduced for populations when grown in the hillside site relative to the floodplain site, suggesting that stress acts to reduce the expression of genetic variance and the potential to respond to selection there. Consistent reductions in heritability associated with more stressful environments suggest that populations invading such sites may undergo little adaptive differentiation and be more prone to local extinction.     

Small‐scale spatial variation in evolvability for life‐history traits in the storm petrel

The evolutionary potential in the timing of recruitment and reproduction may be crucial for the ability of populations to buffer against environmental changes, allowing them to avoid unfavourable breeding conditions. The evolution of a trait in a local population is determined by its heritability and selection. In the present study, we performed pedigree‐based quantitative genetic analyses for two life‐history traits (recruiting age and laying date) using population data of the storm petrel over an 18‐year period in two adjacent breeding colonies (only 150 m apart) that share the same environmental conditions. In both traits, natal colony effect was the main source of the phenotypic variation among individuals, and cohort variance for recruitment age and additive genetic variance for laying date were natal colony‐specific. We found significant heritability only in laying date and, more specifically, only in birds born in one of the colonies. The difference in genetic variance between the colonies was statistically significant. Interestingly, selection on earlier breeding birds was detected only in the colony in which heritable variation in laying date was found. Therefore, local evolvability for a life‐history trait may vary within a unexpectedly small spatial scale, through the diversifying natural selection and insulating gene flow. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 439–446.     

The maintenance of heritable variation through social competition

The paradoxical persistence of heritable variation for fitness-related traits is an evolutionary conundrum that remains a preeminent problem in evolutionary biology. Here we describe a simple mechanism in which social competition results in the evolutionary maintenance of heritable variation for fitness related traits. We demonstrate this mechanism using a genetic model with two primary assumptions: the expression of a trait depends upon success in social competition for limited resources; and competitive success of a genotype depends on the genotypes that it competes against. We find that such social competition generates heritable (additive) genetic variation for "competition-dependent" traits. This heritable variation is not eroded by continuous directional selection because, rather than leading to fixation of favored alleles, selection leads instead to allele frequency cycling due to the concerted coevolution of the social environment with the effects of alleles. Our results provide a mechanism for the maintenance of heritable variation in natural populations and suggest an area for research into the importance of competition in the genetic architecture of fitness related traits.     

Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae: no evidence for trade-offs

Parasitoids are an important mortality factor for insects. Susceptibility to parasitoids should thus be under strong negative selection. Nevertheless, ample genetic variation for susceptibility to parasitoids is commonly observed in natural populations, suggesting that trade-offs may constrain the evolution of reduced susceptibility. This can be studied by assessing genetic variation for susceptibility and its covariation with other components of fitness. In a set of 17 clones of the peach potato aphid, Myzus persicae, for which good estimates of heritable variation for life-history traits were available, we found significant clonal variation for susceptibility to two of their common parasitoids: Aphidius colemani and Diaeretiella rapae. One clone, the only one harbouring a facultative endosymbiotic bacterium, Regiella insecticola, was entirely resistant to both parasitoids. Susceptibilities to the two parasitoids exhibited a positive genetic correlation close to unity, implying a general mechanism of defence. However, the susceptibility to parasitoids was uncorrelated to the clones' fecundity or rate of increase, providing no evidence for costs of the ability to resist parasitoids.     

Heritability of age at first birth in captive olive baboons

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

Natural selection on female life-history traits in relation to socio-economic class in pre-industrial human populations

Life-history theory predicts that resource scarcity constrains individual optimal reproductive strategies and shapes the evolution of life-history traits. In species where the inherited structure of social class may lead to consistent resource differences among family lines, between-class variation in resource availability should select for divergence in optimal reproductive strategies. Evaluating this prediction requires information on the phenotypic selection and quantitative genetics of life-history trait variation in relation to individual lifetime access to resources. Here, we show using path analysis how resource availability, measured as the wealth class of the family, affected the opportunity and intensity of phenotypic selection on the key life-history traits of women living in pre-industrial Finland during the 1800s and 1900s. We found the highest opportunity for total selection and the strongest selection on earlier age at first reproduction in women of the poorest wealth class, whereas selection favoured older age at reproductive cessation in mothers of the wealthier classes. We also found clear differences in female life-history traits across wealth classes: the poorest women had the lowest age-specific survival throughout their lives, they started reproduction later, delivered fewer offspring during their lifetime, ceased reproduction younger, had poorer offspring survival to adulthood and, hence, had lower fitness compared to the wealthier women. Our results show that the amount of wealth affected the selection pressure on female life-history in a pre-industrial human population.     

PLEIOTROPY CAUSES LONG-TERM GENETIC CONSTRAINTS ON LIFE-HISTORY EVOLUTION IN BRASSICA RAPA

Fundamental, long-term genetic trade-offs constrain life-history evolution in wild crucifer populations. I studied patterns of genetic constraint in Brassica rapa by estimating genetic correlations among life-history components by quantitative genetic analyses among ten wild populations, and within four populations. Genetic correlations between age and size at first reproduction were always greater than +0.8 within and among all populations studied. Although quantitative genetics might provide insight about genetic constraints if genetic parameters remain approximately constant, little evidence has been available to determine the constancy of genetic correlations. I found strong and consistent estimates of genetic correlations between life-history components, which were very similar within four natural populations. Population differentiation also showed these same trade-offs, resulting from long-term genetic constraint. For some traits, evolutionary changes among populations were incompatible with a model of genetic drift. Historical patterns of natural selection were inferred from population differentiation, suggesting that correlated response to selection has caused some traits to evolve opposite to the direct forces of natural selection. Comparison with Arabidopsis suggests that these life-history trade-offs are caused by genes that regulate patterns of resource allocation to different components of fitness. Ecological and energetic models may correctly predict these trade-offs because there is little additive genetic variation for rates of resource acquisition, but resource allocation is genetically variable.     

Resource-allocation rules and the heritability of traits

I hypothesize that the heritability of a trait, and thus its evolutionary responsiveness to natural selection, should be positively related to the priority with which resources are allocated to that trait. Low-priority traits are more sensitive to environmental effects, thus reducing the relative effect of genetic differences on phenotypic variation of these traits. This allocation-priority hypothesis explains why life-history traits, such as those involving growth and reproduction, generally have lower heritabilities than higher-priority morphological and physiological traits related to body maintenance. This hypothesis also shows how an organism-centered approach, as used in physiological ecology, can contribute to the development of evolutionary theory.     

Consequences of hierarchical allocation for the evolution of life-history traits

Resource allocation within individuals may often be hierarchical, and this may have important effects on genetic correlations and on trait evolution. For example, organisms may divide energy between reproduction and somatic growth and then subdivide reproductive resources. Genetic variation in allocation to pathways early in such hierarchies (e.g., reproduction) can cause positive genetic correlations between traits that trade off (e.g., offspring size and number) because some individuals invest more resources in reproduction than others. We used quantitative-genetic models to explore the evolutionary implications of allocation hierarchies. Our results showed that when variation in allocation early in the hierarchy exceeds subsequent variation in allocation, genetic covariances and initial responses to selection do not reflect trade-offs occurring at later levels in the hierarchy. This general pattern was evident for many starting allocations and optima and for whether traits contributed multiplicatively or additively to fitness. Finally, artificial selection on a single trait revealed masked trade-offs when variation in early allocation was comparable to subsequent variation in allocation. This result confirms artificial selection as a powerful, but not foolproof, method of detecting trade-offs. Thus, allocation hierarchies can profoundly affect life-history evolution by causing traits to evolve in the opposite direction to that predicted by trade-offs.     

The prediction of adaptive evolution: empirical application of the secondary theorem of selection and comparison to the breeder's equation

Adaptive evolution occurs when fitness covaries with genetic merit for a trait (or traits). The breeder's equation (BE), in both its univariate and multivariate forms, allows us to predict this process by combining estimates of selection on phenotype with estimates of genetic (co)variation. However, predictions are only valid if all factors causal for trait-fitness covariance are measured. Although this requirement will rarely (if ever) be met in practice, it can be avoided by applying Robertson's secondary theorem of selection (STS). The STS predicts evolution by directly estimating the genetic basis of trait-fitness covariation without any explicit model of selection. Here we apply the BE and STS to four morphological traits measured in Soay sheep (Ovis aries) from St. Kilda. Despite apparently positive selection on heritable size traits, sheep are not getting larger. However, although the BE predicts increasing size, the STS does not, which is a discrepancy that suggests unmeasured factors are upwardly biasing our estimates of selection on phenotype. We suggest this is likely to be a general issue, and that wider application of the STS could offer at least a partial resolution to the common discrepancy between naive expectations and observed trait dynamics in natural populations.