Quantitative trait and allozyme divergence in the Greenfinch (Carduelis chloris, Aves: Fringillidae)

Quantitative trait divergence and variability among 12 greenfinch populations across continental Europe was examined and compared to divergence in neutral genetic markers (allozymes). The added among locality variance component for 16 skeletal traits was large (mean 28%, range 4–48%) equalling a divergence of up to three SD units. The divergence in quantitative traits (Qst = 0.04-0.48) greatly exceeded that in alloymes (F_ST= 0.01-0.07), indicating the differentiation in quantitative traits to be larger than expected by mutation and drift alone. This conclusion was consistent also with results from the multivariate approach of Rogers & Harpending. However, genetic and morphometric distances between populations were positively correlated, even when controlling for the geographic distance separating pairs of populations. In concordance with Bergmann's rule, most traits were strongly and positively correlated with latitude, indicating latitudinally ordered genetic or/and environmental effects. However, the correlation between lower mandible width and latitude was strongly negative, demonstrating an inverse relationship between beak size and body size across the populations. These results are interpreted to reflect the re-colonization of history of northern Europe (genetic and geographic distances correlated) which has been paralleled by selection acting on quantitative traits (Q_ST>F_ST)- In particular, the counter-gradient variation in beak width, a functionally important trait, is suggestive of an adaptive basis for quantitative trait divergence.     

The quantitative genetic basis of adaptive divergence in the moor frog (Rana arvalis) and its implications for gene flow

Knowledge on the relative contribution of direct genetic, maternal and environmental effects to adaptive divergence is important for understanding the drivers of biological diversification. The moor frog (Rana arvalis) shows adaptive divergence in embryonic and larval fitness traits along an acidification gradient in south-western Sweden. To understand the quantitative genetic basis of this divergence, we performed reciprocal crosses between three divergent population pairs and reared embryos and larvae at acid and neutral pH in the laboratory. Divergence in embryonic acid tolerance (survival) was mainly determined by maternal effects, whereas the relative contributions of maternal, additive and nonadditive genetic effects in larval life-history traits differed between traits, population pairs and rearing environments. These results emphasize the need to investigate the quantitative genetic basis of adaptive divergence in multiple populations and traits, as well as different environments. We discuss the implications of our findings for maintenance of local adaptation in the context of migrant and hybrid fitness.     

Population‐genomic approach reveals adaptive floral divergence in discrete populations of a hawk moth‐pollinated violet

Local adaptation to contrasting biotic or abiotic environments is an important evolutionary step that presumably precedes floral diversification at the species level, yet few studies have demonstrated the adaptive nature of intraspecific floral divergence in wild plant populations. We combine a population‐genomic approach with phenotypic information on floral traits to examine whether the differentiation in metric floral traits exhibited by 14 populations of the southern Spanish hawk moth‐pollinated violet Viola cazorlensis reflects adaptive divergence. Screening of many amplified fragment length polymorphism (AFLP) loci using a multiple‐marker‐based neutrality test identified nine outlier loci (2.6% of the total) that departed from neutral expectations and were potentially under selection. Generalized analysis of molecular variance revealed significant relationships between genetic distance and population divergence in three floral traits when genetic distance was based on outlier loci, but not when it was based on neutral ones. Population means of floral traits were closely correlated with population scores on the first principal coordinate axis of the genetic distance matrix using outlier loci, and with the allelic frequencies of four of the outlier loci. Results strongly support the adaptive nature of intraspecific floral divergence exhibited by V. cazorlensis and illustrate the potential of genome scans to identify instances of adaptive divergence when used in combination with phenotypic information.     

NO EFFECT OF ENVIRONMENTAL HETEROGENEITY ON THE MAINTENANCE OF GENETIC VARIATION IN WING SHAPE IN DROSOPHILA MELANOGASTER

Theory suggests that heterogeneous environments should maintain more genetic variation within populations than homogeneous environments, yet experimental evidence for this effect in quantitative traits has been inconsistent. To examine the effect of heterogeneity on quantitative genetic variation, we maintained replicate populations of Drosophila melanogaster under treatments with constant temperatures, temporally variable temperature, or spatially variable temperature with either panmictic or limited migration. Despite observing differences in fitness and divergence in several wing traits between the environments, we did not find any differences in the additive genetic variance for any wing traits among any of the treatments. Although we found an effect of gene flow constraining adaptive divergence between cages in the limited migration treatment, it did not tend to increase within‐population genetic variance relative to any of the other treatments. The lack of any clear and repeatable patterns of response to heterogeneous versus homogeneous environments across several empirical studies suggests that a single general mechanism for the maintenance of standing genetic variation is unlikely; rather, the relative importance of putative mechanisms likely varies considerably from one trait and ecological context to another.     

HOW MUCH OF THE VARIATION IN ADAPTIVE DIVERGENCE CAN BE EXPLAINED BY GENE FLOW? AN EVALUATION USING LAKE‐STREAM STICKLEBACK PAIRS

Abstract How much of the variation in adaptive divergence can be explained by gene flow? The answer to this question should objectively reveal whether gene flow generally places a substantial constraint on evolutionary diversification. We studied multiple independent lake‐stream population pairs of threespine stickleback (Gasterosteus acu‐leatus). For each pair, we quantified adaptive divergence based on morphological traits that have a genetic basis and are subject to divergent selection. We then estimated gene flow based on variation at five unlinked microsatellite loci. We found a consistent and significant pattern for morphological divergence to be positively correlated with genetic divergence and negatively correlated with gene flow. Statistical significance and the amount of variation explained varied within and among traits: 36.1–74.1% for body depth and 11.8–51.7% for gill raker number. Variation within each trait was the result of differences among methods for estimating genetic divergence and gene flow. Variation among traits likely reflects different strengths of divergent selection. We conclude that gene flow has a substantial effect on adaptive divergence in nature but that the magnitude of this effect varies among traits. An alternative explanation is that cause and effect are reversed: adaptive divergence is instead constraining gene flow. This effect seems relatively unimportant for our system because genetic divergence and gene flow were not correlated with ecologically relevant habitat features of lakes (surface area) or streams (width, depth, flow, canopy openness).     

The effect of migration during the divergence

The mean and variance of the number of nucleotide differences were obtained when the ancestral population diverged with migration. The number of nucleotide differences obtained indicates that not only the migration rate but also the period of migration has influence on a population structure. According to the migration rate and the period of migration, populations behave approximately as a single unit, diverged and isolated populations, two populations under equilibrium, or none of them. When sigma m(t) is about one, the variance of the number of nucleotide differences becomes large, where sigma m(t) is the sum of the migration rate for the period of migration. The distribution of the estimated divergence time was also obtained using computer simulations. It was found that the divergence time can be explained by sigma m(t). That is, the divergence time is mostly estimated as the time when sigma m(t) is less than 1.     

The effect of a population bottleneck on the evolution of genetic variance/covariance structure

It is well known that standard population genetic theory predicts decreased additive genetic variance (V(a) ) following a population bottleneck and that theoretical models including interallelic and intergenic interactions indicate such loss may be avoided. However, few empirical data from multicellular model systems are available, especially regarding variance/covariance (V/CV) relationships. Here, we compare the V/CV structure of seventeen traits related to body size and composition between control (60 mating pairs/generation) and bottlenecked (2 mating pairs/generation; average F = 0.39) strains of mice. Although results for individual traits vary considerably, multivariate analysis indicates that V(a) in the bottlenecked populations is greater than expected. Traits with patterns and amounts of epistasis predictive of enhanced V(a) also show the largest deviations from additive expectations. Finally, the correlation structure of weekly weights is not significantly different between control and experimental lines but correlations between necropsy traits do differ, especially those involving the heart, kidney and tail length.     

Migration-induced phenotypic divergence: the migration-selection balance of correlated traits

Genetically correlated traits are known to respond to indirect selection pressures caused by directional selection on other traits. It is however unclear how local adaptation in populations diverging along some phenotypic traits but not others is affected by the joint action of gene flow and genetic correlations among traits. This simulation study shows that although gene flow is a potent constraining mechanism of population adaptive divergence, it may induce phenotypic divergence in traits under homogeneous selection among habitats if they are genetically correlated with traits under divergent selection. This correlated phenotypic divergence is a nonmonotonous function of migration and increases with mutational correlation among traits. It also increases with the number of divergently selected traits provided their genetic autonomy relative to the uniformly selected trait is reduced by specific patterns of genetic covariances: populations with lower effective trait dimensionality are more likely to generate very large correlated divergence. The correlated divergence is likely to be picked up by Q(ST)-F(ST) analysis of population genetic differentiation and be erroneously ascribed to adaptive divergence under divergent selection. This study emphasizes the necessity to understand the interaction between selection and the genetic basis of adaptation in a multivariate rather than univariate context.     

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.     

PREY ADAPTATION AS A CAUSE OF PREDATOR-PREY CYCLES

We analyze simple models of predator-prey systems in which there is adaptive change in a trait of the prey that determines the rate at which it is captured by searching predators. Two models of adaptive change are explored: (1) change within a single reproducing prey population that has genetic variation for vulnerability to capture by the predator; and (2) direct competition between two independently reproducing prey populations that differ in their vulnerability. When an individual predator's consumption increases at a decreasing rate with prey availability, prey adaptation via either of these mechanisms may produce sustained cycles in both species' population densities and in the prey's mean trait value. Sufficiently rapid adaptive change (e.g., behavioral adaptation or evolution of traits with a large additive genetic variance), or sufficiently low predator birth and death rates will produce sustained cycles or chaos, even when the predator-prey dynamics with fixed prey capture rates would have been stable. Adaptive dynamics can also stabilize a system that would exhibit limit cycles if traits were fixed at their equilibrium values. When evolution fails to stabilize inherently unstable population interactions, selection decreases the prey's escape ability, which further destabilizes population dynamics. When the predator has a linear functional response, evolution of prey vulnerability always promotes stability. The relevance of these results to observed predator-prey cycles is discussed.     

Independent axes of genetic variation and parallel evolutionary divergence of opercle bone shape in threespine stickleback

Evolution of similar phenotypes in independent populations is often taken as evidence of adaptation to the same fitness optimum. However, the genetic architecture of traits might cause evolution to proceed more often toward particular phenotypes, and less often toward others, independently of the adaptive value of the traits. Freshwater populations of Alaskan threespine stickleback have repeatedly evolved the same distinctive opercle shape after divergence from an oceanic ancestor. Here we demonstrate that this pattern of parallel evolution is widespread, distinguishing oceanic and freshwater populations across the Pacific Coast of North America and Iceland. We test whether this parallel evolution reflects genetic bias by estimating the additive genetic variance-covariance matrix (G) of opercle shape in an Alaskan oceanic (putative ancestral) population. We find significant additive genetic variance for opercle shape and that G has the potential to be biasing, because of the existence of regions of phenotypic space with low additive genetic variation. However, evolution did not occur along major eigenvectors of G, rather it occurred repeatedly in the same directions of high evolvability. We conclude that the parallel opercle evolution is most likely due to selection during adaptation to freshwater habitats, rather than due to biasing effects of opercle genetic architecture.     

Replicated evolution of integrated plastic responses during early adaptive divergence

Colonization of a novel environment is expected to result in adaptive divergence from the ancestral population when selection favors a new phenotypic optimum. Local adaptation in the new environment occurs through the accumulation and integration of character states that positively affect fitness. The role played by plastic traits in adaptation to a novel environment has generally been ignored, except for variable environments. We propose that if conditions in a relatively stable but novel environment induce phenotypically plastic responses in many traits, and if genetic variation exists in the form of those responses, then selection may initially favor the accumulation and integration of functionally useful plastic responses. Early divergence between ancestral and colonist forms will then occur with respect to their plastic responses across the gradient bounded by ancestral and novel environmental conditions. To test this, we compared the magnitude, integration, and pattern of plastic character responses in external body form induced by shallow versus open water conditions between two sunfish ecomorphs that coexist in four postglacial lakes. The novel sunfish ecomorph is present in the deeper open water habitat, whereas the ancestral ecomorph inhabits the shallow waters along the lake margin. Plastic responses by open water ecomorphs were more correlated than those of their local shallow water ecomorph in two of the populations, whereas equal levels of correlated plastic character responses occurred between ecomorphs in the other two populations. Small but persistent differences occurred between ecomorph pairs in the pattern of their character responses, suggesting a recent divergence. Open water ecomorphs shared some similarities in the covariance among plastic responses to rearing environment. Replication in the form of correlated plastic responses among populations of open water ecomorphs suggests that plastic character states may evolve under selection. Variation between ecomorphs and among lake populations in the covariance of plastic responses suggests the presence of genetic variation in plastic character responses. In three populations, open water ecomorphs also exhibited larger plastic responses to the environmental gradient than the local shallow water ecomorph. This could account for the greater integration of plastic responses in open water ecomorphs in two of the populations. This suggests that the plastic responses of local sunfish ecomorphs can diverge through changes in the magnitude and coordination of plastic responses. Although these results require further investigation, they suggest that early adaptive evolution in a novel environment can include changes to plastic character states. The genetic assimilation of coordinated plastic responses could result in the further, and possibly rapid, divergence of such populations and could also account for the evolution of genes of major effect that contribute to suites of phenotypic differences between divergent populations.     

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.     

Q ST MEETS THE G MATRIX: THE DIMENSIONALITY OF ADAPTIVE DIVERGENCE IN MULTIPLE CORRELATED QUANTITATIVE TRAITS

The Q _ST– F _ST comparison has become an increasingly common method for inferring adaptive quantitative trait divergence among populations. For cases in which there is divergence in multiple traits, most studies have applied the method by performing multiple univariate Q _ST– F _ST comparisons. However, because traits are often genetically correlated, such univariate analyses are likely to paint a simplified picture of adaptive divergence. Here we show how the multivariate analogue of Q _ST, F_STq, which accounts for genetic correlations among traits, can be used to supply a more detailed picture of multitrait divergence. We apply the method to naturally occurring genetic variation for a suite of sexually selected display traits in Drosophila serrata . The analyses suggest the operation of divergent multivariate selection that has influenced multiple independent axes of genetic variance in a sex-specific manner. Finally, we show how a comparison of the components of F_STq, the average within and among population genetic variance–covariance matrices, G_W and G_B, can be used as an additional test of the null expectation of neutral divergence, and allows for an investigation of whether natural populations have diverged along major or minor axes of genetic variance.     

Evolution of morphological differences with moderate genetic correlations among traits as exemplified by two flycatcher species (Ficeduia; Muscicapidae)

Theoretical work on multivariate evolution predicts that genetic correlations can act to constrain the rate at which new adaptive peaks are reached, but there is very limited empirical information available on this issue so far. To evaluate the importance of genetic correlations for evolutionary change, we studied the morphological differences between two flycatcher species (Ficeduia albicollis and F. hypoleuca) using both univariate and multivariate quantitative genetic models. Comparison of the results obtained using these different models revealed that even relatively low genetic correlations between traits will considerably increase the net selection forces needed for evolutionary changes in morphology. In particular, the divergence in wing and tail length, which are positively genetically correlated, would require a considerable amount of antagonistic selection. Because of the genetic correlations, strong selection will be needed to retain certain traits unchanged while others are changing. Based on these results, we argue that it is unlikely that small morphological differences such as between these two species could have evolved during a short (200 years) time period, i.e. the period of sympatry of these species in Sweden. These findings support the hypothesis that even relatively low genetic correlations may constrain short-term adaptive evolution in natural populations.     

Q(St) meets the G matrix: the dimensionality of adaptive divergence in multiple correlated quantitative traits.

The Q(ST)-F(ST) comparison has become an increasingly common method for inferring adaptive quantitative trait divergence among populations. For cases in which there is divergence in multiple traits, most studies have applied the method by performing multiple univariate Q(ST)-F(ST) comparisons. However, because traits are often genetically correlated, such univariate analyses are likely to paint a simplified picture of adaptive divergence. Here we show how the multivariate analogue of Q(ST), F(STq), which accounts for genetic correlations among traits, can be used to supply a more detailed picture of multitrait divergence. We apply the method to naturally occurring genetic variation for a suite of sexually selected display traits in Drosophila serrata. The analyses suggest the operation of divergent multivariate selection that has influenced multiple independent axes of genetic variance in a sex-specific manner. Finally, we show how a comparison of the components of F(STq), the average within and among population genetic variance-covariance matrices, G(W) and G(B), can be used as an additional test of the null expectation of neutral divergence, and allows for an investigation of whether natural populations have diverged along major or minor axes of genetic variance.     

Quantitative genetic variation of leaf size and shape in a mixed diploid and triploid population of Populus

In the interspecific cross of Populus trichocarpa x P. deltoides, unexpected simultaneous occurrence of diploid hybrids and triploid hybrids (with two alleles from the female parent and one from the male parent at each locus) led us to examine the evolutionary genetic significance of this phenomenon. As expected, leaf size and shape of the triploid progeny are closer to the female P. trichocarpa than male P. deltoides parent. Although the pure triploid progeny population did not have higher genetic variance in leaf traits than the pure diploid population, the former appears to hide much non-additive genetic variance and display strong genetic control over the phenotypic plasticity of leaf traits. It is suggested that the cryptic non-additive variance, especially epistasis, can be released when a population is disturbed by changes in the environment. A mixed diploid and triploid progeny population combines phenotypic and genetic characteristics of both pure hybrids and is considered to be of adaptive significance for populars to survive and evolve in a fluctuating environment. The significant effect due to general and specific combining ability differences at the population level suggests that the population divergence of these two species is under additive and non-additive genetic control.     

The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs

Adaptive evolutionary change is contingent on variation and selection; thus, understanding adaptive divergence and ultimately speciation requires information on both the genetic basis of adaptive traits as well as an understanding of the role of divergent natural selection on those traits. The lake whitefish (Coregonus clupeaformis) consists of several sympatric "dwarf" (limnetic) and normal (benthic) species pairs that co-inhabit northern postglacial lakes. These young species pairs have evolved independently and display parallelism in life history, behavioral, and morphological divergence associated with the use of distinct trophic resources. We identified phenotype-environment associations and determined the genetic architecture and the role of selection modulating population genetic divergence in sympatric dwarf and normal lake whitefish. The genetic architecture of 9 adaptive traits was analyzed in 2 hybrid backcrosses individually phenotyped throughout their life history. Significant quantitative trait loci (QTL) were associated with swimming behavior (habitat selection and predator avoidance), growth rate, morphology (condition factor and gill rakers), and life history (onset of maturity and fecundity). Genome scans among 4 natural sympatric pairs, using loci segregating in the map, revealed a signature of selection for 24 loci. Loci exhibiting a signature of selection were associated with QTL relative to other regions of the genome more often than expected by chance alone. Two parallel QTL outliers for growth and condition factor exhibited segregation distortion in both mapping families, supporting the hypothesis that adaptive divergence contributing to parallel reductions of gene flow among natural populations may cause genetic incompatibilities. Overall, these findings offer evidence that the genetic architecture of ecological speciation is associated with signatures of selection in nature, providing strong support for the hypothesis that divergent natural selection is currently maintaining adaptive differentiation and promoting ecological speciation in lake whitefish species pairs.     

Effects of Population Size and Selection Intensity on Correlated Responses to Selection for Postweaning Gain in Mice

Correlated responses to selection for postweaning gain in mice were studied to determine the influence of population size and selection intensity. Correlated traits measured were three-, six- and eight-week body weights, litter size, twelve-day litter weight, proportion infertile matings and two indexes of reproductive performance. In general, the results agreed with observations made on direct response: correlated responses in the body weight traits and litter size increased as (1) selection intensity increased and (2) effective population size increased. Correlated responses in the body weight traits and litter size were positive in the large population size lines (16 pairs), as expected from the positive genetic correlation between these traits and postweaning gain. However, several negative correlated responses were observed at small population sizes (one and two pairs). Within each level of selection intensity, traits generally associated with fitness tended to decline most in the very small populations (one and two pairs) and in the large populations (16 pairs) for apparently different reasons. The fitness decline at the small effective population sizes was attributable to inbreeding depression. In contrast, it was postulated that the fitness decline at the large effective population size was due to selection moving the population mean for body weight and a trait positively correlated genetically with body weight (i.e., percent body fat) away from an optimum.     

Does natural selection promote population divergence? A comparative analysis of population structure using amplified fragment length polymorphism markers and quantitative traits

Divergent natural selection is considered an important force in plant evolution leading to phenotypic differentiation between populations exploiting different environments. Extending an earlier greenhouse study of population differentiation in the selfing annual plant Senecio vulgaris, we estimated the degree of population divergence in several quantitative traits related to growth and life history and compared these estimates with those based on presumably neutral molecular markers (amplified fragment length polymorphisms; AFLPs). This approach allowed us to disentangle the effects of divergent selection from that of other evolutionary forces (e.g. genetic drift). Five populations were examined from each of two habitat types (ruderal and agricultural habitats). We found a high proportion of total genetic variance to be among populations, both for AFLP markers (phiST = 0.49) and for quantitative traits (range of QST: 0.26-0.77). There was a strong correlation between molecular and quantitative genetic differentiation between pairs of populations (Mantel's r = 0.59). However, estimates of population differentiation in several quantitative traits exceeded the neutral expectation (estimated from AFLP data), suggesting that divergent selection contributed to phenotypic differentiation, especially between populations from ruderal and agricultural habitats. Estimates of within-population variation in AFLP markers and quantitative genetic were poorly correlated, indicating that molecular marker data may be of limited value to predict the evolutionary potential of populations of S. vulgaris.