Population divergence and morphometric integration in the greenfinch (Carduelis chloris) – evolution against the trajectory of least resistance?

Theory predicts that genetic and phenotypic correlations among traits may direct the process of short-term evolution by limiting the directions of variation available to natural selection to act on. We studied correlations between 14 skeletal traits in 10 geographically distinct and relatively young greenfinch (Carduelis chloris) populations to unravel whether the divergence among populations has occurred into directions predicted by the within-population correlations (cf. drift/correlated responses models), or whether it is better explained by ‘adaptive’ models, which predict no necessary association between within- and among-population correlations (allometries). We found that the within-population character correlations (or covariances) did not predict character divergence between populations. This was because the first eigenvector of the among-population correlation/covariance matrix, summarizing the major dimension of divergence, was a bipolar body:beak dimension, and distinct from the (≈ isometric) first eigenvector of within-population matrix. Hence, as the divergence among greenfinch populations cannot be satisfactorily accommodated by drift/correlated response models, an adaptive basis for divergence is suggested. The second major axis of within-population variation was a classical ‘group size’ factor revealing that beak size was more or less free to vary independently of body size. Consequently, even if the divergence among populations cannot be simply accommodated to expectations of drift and correlated response models, it is striking that the most pronounced size-independent (nonallometric) changes had occurred along the second largest dimension of variance. This could mean that selection pressures which shape integration within populations are the same as those that cause divergence among populations. A relaxed beak:body integration could also occur as a result of species level selection favouring taxa in which independent evolution of beak and body is made possible.     

TESTING LIFE-HISTORY PLEIOTROPY IN CAENORHABDITIS ELEGANS

Abstract Much life-history theory assumes that alleles segregating in natural populations pleiotropically affect life-history traits. This assumption, while plausible, has rarely been tested directly. Here we investigate the genetic relationship between two traits often suggested to be connected by pleiotropy: maternal body size and fertility. We carry out a quantitative trait locus (QTL) analysis on two isolates of the free-living nematode Caenorhabditis elegans , and identify two body size and three fertility QTLs. We find that one of the fertility QTLs colocalizes with the two body size QTLs on Chromosome IV. Further analysis, however, shows that these QTLs are genetically separable. Thus, none of the five body size or fertility QTLs identified here shows detectable pleiotropy for the assayed traits. The evolutionary origin of these QTLs, possible candidate loci, and the significance for life-history evolution are discussed.     

The effect of purging on sexually selected traits through antagonistic pleiotropy with survival

Sexually selected traits are expected to evolve to a point where their positive effect on reproductive success is counterbalanced by their negative effect on survival. At the genetic level, such a trade-off implies antagonistic pleiotropy between survival and the expression of sexually selected traits. Yet, the consequences of such a genetic architecture have been largely overlooked in studies examining how inbreeding influences sexually selected traits. These studies have solely interpreted their results as an effect of increased homozygosity. An alternative, however, is that purging of recessive alleles deleterious for survival when inbreeding increases can negatively affect the expression of sexually selected traits through antagonistic pleiotropy. We tested this hypothesis by analyzing the effects of inbreeding on several male ornaments and life-history traits across 20 captive populations of guppies (Poecilia reticulata) with varying levels of inbreeding. Only one ornament, orange area, decreased in its expression with an increasing level of inbreeding. This was most likely due to purging because we found no within-population relationship between orange area and the inbreeding coefficient. We further tested this hypothesis by crossing unrelated individuals from the four most inbred populations, creating a group of individuals with purged genomes but restored heterozygosity. Restoration of heterozygosity only slightly increased orange area, confirming that the decrease in orange area in the inbred populations most likely resulted from purging. These results support previous studies suggesting the existence of antagonistic pleiotropy between ornament expression and survival.     

Evolution of pleiotropic alleles for maturation and size as a consequence of predation

Understanding life-history evolution requires knowledge about genetic interactions, physiological mechanisms and the nature of selection. For platyfish, Xiphophorus maculatus, extensive information is available about genetic and physiological mechanisms influencing life-history traits. In particular, alleles at the pituitary locus have large and antagonistic effects on age and size at sexual maturation. To examine how predation affects the evolution of these antagonistic traits, I examined pituitary allele evolution in experimental populations differing in predation risk. A smaller size, earlier maturation allele increased in frequency when predators were absent, while a larger size, later maturation allele increased in frequency when predators were present. Thus, predation favours alleles for larger size, at the cost of later maturation and reproduction. These findings are interesting for several reasons. First, predation is often predicted to favour early reproduction at smaller sizes. Second, few studies have shown how selection acts on alleles that affect age and size at sexual maturation. Finally, many studies assume that trade-offs between these life-history traits result from antagonistic pleiotropy, with alleles that positively affect one trait negatively affecting another, yet this is rarely known. This study unequivocally demonstrates that genetically based trade-offs affect life-history evolution in platyfish.     

Evolution of the G-matrix in life history traits in the common frog during a recent colonisation of an island system

Studies of genetic correlations between traits that ostensibly channel the path of evolution away from the direction of natural selection require information on key aspects such as ancestral phenotypes, the duration of adaptive evolution, the direction of natural selection, and genetic covariances. In this study we provide such information in a frog population system. We studied adaptation in life history traits to pool drying in frog populations on islands of known age, which have been colonized from a mainland population. The island populations show strong local adaptation in development time and size. We found that the first eigenvector of the variance–covariance matrix (g _max) had changed between ancestral mainland populations and newly established island populations. Interestingly, there was no divergence in g _max among island populations that differed in their local adaptation in development time and size. Thus, a major change in the genetic covariance of life-history traits occurred in the colonization of the island system, but subsequent local adaptation in development time took place despite the constraints imposed by the genetic covariance structure.     

QUANTITATIVE GENETICS OF SURVIVAL AND GROWTH IN IMPATIENS CAPENSIS

When variation in life-history characters is caused by many genes of small effect, then quantitative-genetic parameters may quantify constraints on rate and direction of microevolutionary change. I estimated heritabilities and genetic correlations for 16 life-history and morphological characters in two populations of Impatiens capensis, a partially self-pollinating herbaceous annual. The Madison population had little or no additive genetic variance for any of these characters, while the Milwaukee population had significant narrowsense heritabilities and genetic correlations for several traits, including adult size, which is highly correlated with fitness. All genetic correlations among fitness components were positive, hence there is no evidence for antagonistic pleiotropy among these traits. Dissimilarity of heritabilities in the two populations supports theoretical predictions that long-term changes in genetic variance-covariance patterns may occur when population sizes are small and selection is strong, as may occur in many plant species.     

The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus

Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait‐specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high‐throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy‐mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.     

Causes of covariation of phenotypic traits among populations

Morphological and life-history traits often vary among populations of a species. Traits generally do not vary independently, but show patterns of covariation that can arise from genetic and environmental influences on phenotype. Covariance of traits may arise at an among-population level when genetically influenced traits diverge among populations in a correlated manner. Genetic correlations caused by pleiotropy and/or gene linkage can cause traits to evolve together, but among-population covariance can also arise among traits that are not genetically correlated. For example, “selective covariance” can arise when natural selection directly causes correlated change in a suite of traits. Similarly, mutation, migration, and drift may also sometimes cause correlated genetic changes among populations. Because covariation of traits among populations can arise by several different processes, the evolution of suites of traits must be interpreted with great caution. We discuss the sources of among-population covariance and illustrate one approach to identifying the sources' using data on floral traits of Dalechampia scandens (Euphorbiaceae).     

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.     

Evolutionary response to selection on clutch size in a long-term study of the mute swan

Life-history traits in wild populations are often regarded as being subject to directional selection, and the existence of substantial variation and microevolutionary stasis of these characters is therefore a problem in need of explanation. Avian clutch size is an archetypal life-history trait in this context, and many studies have sought to test explanations for stasis in clutch size. Surprisingly, there are many fewer studies that used long-term data to ask how selection acts on clutch size, particularly in a multivariate framework. In this article, we report selection, inheritance, and evolution of clutch size over 25 years in a colony of mute swans using a multivariate quantitative genetic framework to control for correlations with breeding time. We show that clutch size is influenced by both additive genetic and permanent environmental effects and that selection acts on clutch size in combination with breeding time. Natural selection on clutch size is strongly directional, favoring larger clutches, and we observe an increase in clutch size of 0.35 standard deviations, consistent with the expected response based on selection and inheritance of clutch size. We hypothesize that these changes result from recent relaxation of food constraints and predation risks experienced by this colony.     

Pleiotropic quantitative trait loci contribute to population divergence in traits associated with life-history variation in Mimulus guttatus

Evolutionary biologists seek to understand the genetic basis for multivariate phenotypic divergence. We constructed an F2 mapping population (N = 539) between two distinct populations of Mimulus guttatus. We measured 20 floral, vegetative, and life-history characters on parents and F1 and F2 hybrids in a common garden experiment. We employed multitrait composite interval mapping to determine the number, effect, and degree of pleiotropy in quantitative trait loci (QTL) affecting divergence in floral, vegetative, and life-history characters. We detected 16 QTL affecting floral traits; 7 affecting vegetative traits; and 5 affecting selected floral, vegetative, and life-history traits. Floral and vegetative traits are clearly polygenic. We detected a few major QTL, with all remaining QTL of small effect. Most detected QTL are pleiotropic, implying that the evolutionary shift between these annual and perennial populations is constrained. We also compared the genetic architecture controlling floral trait divergence both within (our intraspecific study) and between species, on the basis of a previously published analysis of M. guttatus and M. nasutus. Eleven of our 16 floral QTL map to approximately the same location in the interspecific map based on shared, collinear markers, implying that there may be a shared genetic basis for floral divergence within and among species of Mimulus.     

THE COVARIANCE STRUCTURE OF LIFE-HISTORY CHARACTERS IN DAPHNIA PULEX

The genetic covariance structure for life-history characters in two populations of cyclically parthenogenetic Daphnia pulex indicates considerable positive correlation among important fitness components, apparently at odds with the expectation if antagonistic pleiotropy is the dominant cause of the maintanence of genetic variation. Although there is no genetic correlation between offspring size and offspring number, present growth and present reproduction are both strongly positively correlated genetically with future reproduction, and early maturity is genetically correlated with larger clutch size. Although the ubiquity of antagonistic pleiotropy has been recently questioned, there are peculiarities of cyclical parthenogenesis that could lead to positive life-history covariance even when negative covariance would be expected in a similar sexual species. These include the influence of nonadditive gene action on evolution in clonally reproducing organisms, and the periodic release of hidden genetic variance within populations of cyclical parthenogens. Examination of matrix similarity, using the bootstrap for distribution-free hypothesis testing, reveals no evidence to suggest that the genetic covariance matrices differ between the populations. However, there is considerable evidence that the phenotypic and environmental covariance matrices differ between populations. These results indicate approximate stability of the genetic covariance matrix within species, an important assumption of many phenotypic evolution models, but should caution against the use of phenotypic in place of genetic covariance matrices.     

Rapid divergence of genetic variance-covariance matrix within a natural population

The matrix of genetic variances and covariances (G matrix) represents the genetic architecture of multiple traits sharing developmental and genetic processes and is central for predicting phenotypic evolution. These predictions require that the G matrix be stable. Yet the timescale and conditions promoting G matrix stability in natural populations remain unclear. We studied stability of the G matrix in a 20-year evolution field experiment, where a population of the cosmopolitan parthenogenetic soil nematode Acrobeloides nanus was subjected to drift and divergent selection (benign and stress environments). Selection regime did not influence the level of absolute genetic constraints: under both regimes, two genetic dimensions for three life-history traits were identified. A substantial response to selection in principal components structure and in general matrix pattern was indicated by three statistical methods. G structure was also influenced by drift, with higher divergence under benign conditions. These results show that the G matrix might evolve rapidly in natural populations. The observed high dynamics of G structure probably represents the general feature of asexual species and limits the predictive power of G in phenotypic evolution analyses.     

DIFFERENTIATION AMONG POPULATIONS OF TETRAPLOID GRINDELIA CAMPORUM

Ten populations of 4N Grindelia camporum (Asteraceae) were investigated in a common-garden study of phenotypic and genetic variability. This species is a long-lived perennial herb and an obligate outcrosser which would be expected to display considerable gene flow among populations based on its life-history traits. Each of the 17 morphological, phenological, and physiological traits examined showed significant differences between populations. Average within-population heritability was 0.39. The variation between populations averaged 3.3 times the variation within populations, indicating that the populations are well-differentiated for each of the 17 traits. Two possible explanations for the differentiation are given: populations may have diverged from a common ancestor in very little geologic time, or the species may have a polytopic origin.     

Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback

Parallel (or convergent) evolution provides strong evidence for a deterministic role of natural selection: similar phenotypes evolve when independent populations colonize similar environments. In reality, however, independent populations in similar environments always show some differences: some nonparallel evolution is present. It is therefore important to explicitly quantify the parallel and nonparallel aspects of trait variation, and to investigate the ecological and genetic explanations for each. We performed such an analysis for threespine stickleback (Gasterosteus aculeatus) populations inhabiting lake and stream habitats in six independent watersheds. Morphological traits differed in the degree to which lake-stream divergence was parallel across watersheds. Some aspects of this variation were correlated with ecological variables related to diet, presumably reflecting the strength and specifics of divergent selection. Furthermore, a genetic scan revealed some markers that diverged between lakes and streams in many of the watersheds and some that diverged in only a few watersheds. Moreover, some of the lake-stream divergence in genetic markers was associated within some of the lake-stream divergence in morphological traits. Our results suggest that parallel evolution, and deviations from it, are primarily the result of natural selection, which corresponds in only some respects to the dichotomous habitat classifications frequently used in such studies.     

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.     

Indirect selection of thermal tolerance during experimental evolution of Drosophila melanogaster

Natural selection alters the distribution of a trait in a population and indirectly alters the distribution of genetically correlated traits. Long‐standing models of thermal adaptation assume that trade‐offs exist between fitness at different temperatures; however, experimental evolution often fails to reveal such trade‐offs. Here, we show that adaptation to benign temperatures in experimental populations of Drosophila melanogaster resulted in correlated responses at the boundaries of the thermal niche. Specifically, adaptation to fluctuating temperatures (16–25°C) decreased tolerance of extreme heat. Surprisingly, flies adapted to a constant temperature of 25°C had greater cold tolerance than did flies adapted to other thermal conditions, including a constant temperature of 16°C. As our populations were never exposed to extreme temperatures during selection, divergence of thermal tolerance likely reflects indirect selection of standing genetic variation via linkage or pleiotropy. We found no relationship between heat and cold tolerances in these populations. Our results show that the thermal niche evolves by direct and indirect selection, in ways that are more complicated than assumed by theoretical models.     

Interpreting Geographic Variation in Life-History Traits

The geographic variation in the length of the larval periodand the size at metamorphosis of the wood frog,Rana sylvatica,is examined for populations in the tundra of Canada, the mountainsof Virginia, and the lowlands of Maryland. We argue that theobserved differences in developmental plasticity, heriisbilitiesand genetic covariances of traits among localities result fromdifferential selection pressures in each environment, and arerelated to the physiological constraints inherent in developmentand to the degree of compromise between the timing and sizeat metamorphosis allowed in each environment. In Maryland populationsfitness has been maximized by evolutionary changes in size alone;body size in this population is canalized, has low heritabilityand is highly correlated with juvenile survival relative todevelopmental time. In Canada, minimum developmental time yieldsmaximum fitness; the length of the larval period in this populationis canalized and genetically monomorphic relative to body size.In contrast, fitness in the Virginia populations has been determinedby correlated and pleiotropic effects of genes on both developmentaltime and larval body size, and both traits are equally canalized,affect juvenile survivorship equally and display moderate heritabilities.These results stress the importance of interpreting variationin life-history traits relative to constraints inherent in developmentand those imposed by the environment. Heritability and survivorshipdata support the general notion that fitness traits should havelow levels of additive genetic variation, but also suggest thatantagonistic pleiotropy may act to preserve genetic variationin fitness traits under simultaneous selection, and cautionagainst inferring evolutionary importance of individual traitswithout considering the possible presence of pleiotropy.     

Molecular and quantitative genetic differentiation in European populations of Silene latifolia (Caryophyllaceae)

BACKGROUND AND AIMS: Among-population differentiation in phenotypic traits and allelic variation is expected as a consequence of isolation, drift, founder effects and local selection. Therefore, investigating molecular and quantitative genetic divergence is a pre-requisite for studies of local adaptation in response to selection under variable environmental conditions. METHODS: Among- and within-population variation were investigated in six geographically separated European populations of the white campion, Silene latifolia, both for molecular variation at six newly developed microsatellite loci and for quantitative variation in morphological and life-history traits. To avoid confounding effects of the maternal environment, phenotypic traits were measured on greenhouse-reared F(1) offspring. Tests were made for clinal variation, and the correlations among molecular, geographic and phenotypic distances were compared with Mantel tests. KEY RESULTS: The six populations of Silene latifolia investigated showed significant molecular and quantitative genetic differentiation. Geographic and phenotypic distances were significantly associated. Age at first flowering increased significantly with latitude and exhibited a Q(st) value of 0.17 in females and 0.10 in males, consistent with adaptation to local environmental conditions. By contrast, no evidence of isolation-by-distance and no significant association between molecular and phenotypic distances were found. CONCLUSIONS: Significant molecular genetic divergence among populations of Silene latifolia, from the European native range is consistent with known limited seed and pollen flow distances, while significant quantitative genetic divergence among populations and clinal variation for age at first flowering suggest local adaptation.     

THE QUANTITATIVE AND MOLECULAR GENETIC ARCHITECTURE OF A SUBDIVIDED SPECIES

In an effort to elucidate the evolutionary mechanisms that determine the genetic architecture of a species, we have analyzed 17 populations of the microcrustacean Daphnia pulex for levels of genetic variation at the level of life-history characters and molecular markers in the nuclear and mitochondrial genomes. This species is highly subdivided, with approximately 30% of the variation for nuclear molecular markers and 50% of the variation for mitochondrial markers being distributed among populations. The average level of genetic subdivision for quantitative traits is essentially the same as that for nuclear markers, which superficially suggests that the life-history characters are diverging at the neutral rate. However, the existence of a strong correlation between the levels of population subdivision and broadsense heritabilities of individual traits argues against this interpretation, suggesting instead that the among-population divergence of some quantitative traits (most notably body size) is being driven by local adaptation to different environments. The fact that the mean phenotypes of the individual populations are also strongly correlated with local levels of homozygosity indicates that variation in local inbreeding plays a role in population differentiation. Rather than being a passive consequence of local founder effects, levels of homozygosity may be selected for directly for their effects on the phenotype (adaptive inbreeding depression). There is no relationship between the levels of variation within populations for molecular markers and quantitative characters, and this is explained by the fact that the average standing genetic variation for life-history characters in this species is equivalent to only 33 generations of variation generated by mutation.