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).     

The role of genetic constraints on the diversification of Iberian taxa of the genus Aquilegia (Ranunculaceae)

The microevolutionary process of adaptive phenotypic differentiation of quantitative traits between populations or closely‐related taxa depends on the response of populations to the action of natural selection. However, this response can be constrained by the structure of the matrix of additive genetic variance and covariance between traits in each population ( G matrix). In the present study, we obtained additive genetic variance and narrow sense heritability for 25 floral and vegetative traits of three subspecies of Aquilegia vulgaris, and one subspecies of Aquilegia pyrenaica through a common garden crossing experiment. For two vegetative and one floral trait, we also obtained the G matrix and genetic correlations between traits in each subspecies. The amount of genetic variation available in wild populations is not responsible for the larger differentiation of vegetative than floral traits found in this group of columbines. However, the low heritability of some traits constrained their evolution because phenotypic variability among taxa was larger for traits with larger heritability. We confirmed that the process of diversification of the studied taxa involved shifts in the G matrix, mainly determined by changes in the genetic covariance between floral and vegetative traits, probably caused by linkage disequilibrium in narrow endemic taxa. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 252–261.     

Comparative floral and vegetative differentiation between two European Aquilegia taxa along a narrow contact zone

As a first step in determining the identity and relative importance of the evolutionary forces promoting the speciation process in two closely related European taxa of Aquilegia, we investigated the levels of morphological variation in floral and vegetative characters over the narrow region where their ranges enter into contact, and evaluate the relative importance of both types of traits in their differentiation. A total of 12 floral and ten vegetative characters were measured on 375 plants belonging to seven A. vulgaris populations and six A. pyrenaica subsp. cazorlensis populations located in southeastern Spain. Floral and vegetative morphological differentiation occur between taxa and among populations within taxa, but only vegetative characters (particularly plant height and leaf petiolule length) contribute significantly to the discrimination between taxa. Differentiation among populations within taxa is mostly explained by variation in floral traits. Consequently, morphological divergence between the two taxa cannot be interpreted as an extension of among-population differences occurring within taxa. Multivariate vegetative, but not floral, similarity between populations could be predicted from geographical distance. Moreover, the key role of certain vegetative traits in the differentiation of A. vulgaris and A. p. cazorlensis could possibly be attributable to the contrasting habitat requirements and stress tolerance strategies of the two taxa. These preliminary findings seem to disagree with the currently established view of the radiation process in the genus Aquilegia in North America, where the differentiation of floral traits seems to have played a more important role.     

The structure of phenotypic variation in gender and floral traits within and among populations of Spergularia marina (Caryophyllaceae)

We sampled four wild populations of the highly autogamous Spergularia marina (Caryophyllaceae) in California to detect and to measure the magnitude of within- and among-population sources of phenotypic variation in gender and floral traits. From flowers and fruits collected from field and greenhouse-raised plants, we measured ovule number, seed number, mean seed mass, pollen production (greenhouse families only), mean pollen grain volume (greenhouse families only), anther number, anther/ovule ratio, pollen/ovule ratio (estimated using different flowers for pollen than for ovules; greenhouse families only), petal number, and petal size. Using greenhouse-raised genotypes, variation among maternal families nested within populations was evaluated for each trait to determine whether populations differ in the degree of maternally transmitted phenotypic variation. For each population, we used 15 greenhouse-raised maternal families to estimate the broad-sense heritability and genetic coefficient of variation of each floral trait. The magnitude and statistical significance of broad-sense heritability estimates were trait- and population-specific. Each population was characterized by a different combination of floral traits that expressed significant maternally transmitted (presumably genetic) variation under greenhouse conditions. Flowers representing two populations expressed low levels of maternally transmitted variation (three or fewer of nine measured traits exhibited significant maternal family effects on phenotype), while flowers representing the other two populations exhibited significant maternal family effects on phenotype for five or more traits. Our ability to detect statistically significant differences among the four populations depended upon the conditions under which plants were grown (field vs. greenhouse) and on the floral trait observed. Field-collected flowers exhibited significant differences among population means for all traits except anther number. Flowers sampled from greenhouse-raised maternal families differed among populations for all traits except ovule number, seed number, and petal size. We detected negligible evidence that genetic correlations constrain selection on floral traits in Spergularia marina.     

Adaptive differentiation of quantitative traits in the globally distributed weed, wild radish (Raphanus raphanistrum)

Weedy species with wide geographical distributions may face strong selection to adapt to new environments, which can lead to adaptive genetic differentiation among populations. However, genetic drift, particularly due to founder effects, will also commonly result in differentiation in colonizing species. To test whether selection has contributed to trait divergence, we compared differentiation at eight microsatellite loci (measured as F(ST)) to differentiation of quantitative floral and phenological traits (measured as Q(ST)) of wild radish (Raphanus raphanistrum) across populations from three continents. We sampled eight populations: seven naturalized populations and one from its native range. By comparing estimates of Q(ST) and F(ST), we found that petal size was the only floral trait that may have diverged more than expected due to drift alone, but inflorescence height, flowering time, and rosette formation have greatly diverged between the native and nonnative populations. Our results suggest the loss of a rosette and the evolution of early flowering time may have been the key adaptations enabling wild radish to become a major agricultural weed. Floral adaptation to different pollinators does not seem to have been as necessary for the success of wild radish in new environments.     

Testing hypotheses of functional relationships: a comparative survey of correlation patterns among floral traits in five insect-pollinated plants

To test hypotheses on the evolution of functional relationships, phenotypic correlations among floral traits were estimated in five species of insect-pollinated plants. The species studied were wild radish (Raphanus raphanistrum), canola (Brassica napus), phlox (Phlox divaricata), dame's rocket (Hesperis matronalis), and black mustard (Brassica nigra). Six floral traits were measured on each species. In three of the five species the correlations between the filaments and corolla tube were significantly greater than the other floral correlations. This result is consistent with the hypothesis that selection for proper anther placement to enhance pollination has increased the filament-corolla tube correlations in these three species. In contrast, none of the species showed evidence of selection for an optimal stigma placement; the correlations between the pistil and corolla tube lengths were not greater than the other floral correlations in any of the five species.     

LOW GENIC DIFFERENTIATION AMONG ISOLATED POPULATIONS OF THE CALIFORNIA FAN PALM (WASHINGTONIA FILIFERA)

The purpose of this study was to assess the relative roles of population size and geographic isolation in determining population-genetic structure. Using electrophoretic techniques to quantify allozymic variation at 16 genetic loci, we measured genic variation within and among 16 natural populations of the California fan palm (Washingtonia filifera). Genotypes were determined for every individual in each population so that parametric values rather than sample estimates for measures of genic variability were obtained. Palm populations displayed low levels of within-population variability. The proportion of polymorphic loci and observed heterozygosity were 0.098 and 0.009 per population, respectively. Population size displayed a significant positive correlation with proportion of polymorphic loci, but not with observed heterozygosity. Low levels of genetic differentiation among populations were demonstrated by an F-statistic analysis and the computation of genetic similarity values. A hierarchical analysis of gene diversity revealed that only about 2% of the total gene diversity in W. filifera resides as among-population diversity. Climatic and geological changes since the Pliocene have eliminated widespread palm populations, and the species is presently restricted to isolated locations around the Colorado Desert. Existing populations in southern California are either relicts or recent recolonizations resulting from the dispersal of seeds from a refugium population in Baja California, Mexico. The observed patterns of low within- and low among-population genic diversity seem most consistent with a recent colonization by fan palms. It is hypothesized that stochastic processes reduced levels of genic variability in this refugium population during its formation. Dispersal of seeds from this refugium into suitable habitats in the Colorado Desert would produce populations with low variability and high genetic similarity because of their common ancestry. However, low intrapopulation variability and genetic homogeneity across populations could be the product of uniform selection pressures favoring a narrow array of specialized genotypes in either relict or colonizing populations.     

GENETIC VARIATION,DIFFERENTIATION, AND EVOLUTION IN A SPECIES COMPLEX OF TROPICAL SHRUBS BASED ON ISOZYMIC DATA

An isozyme investigation of the Lisianthius skinneri (Gentianaceae) species complex in central Panama assayed levels of genetic variation within and among isolated populations and was used to reconstruct phylogenetic relationships within the complex. The widespread and low elevation L. skinneri and one derived cloud forest endemic species, L. habuensis, are depauperate in genetic variation. Three other endemic cloud forest species exhibiting larger population sizes and apparently more outcrossed breeding systems have higher levels of heterozygosity but retain low levels of allelic diversity. More than 90% of the genetic variation in the species complex is confined to among-population differentiation rather than witnin-population variation. Isozyme-based relationships within the species complex using both genetic divergence values (Fitch and Margoliash algorithm) and shared allelic states (Nelson and Van Horn algorithm) are identical. This network is not entirely congruent with a previous DNA-based network. Geographical isolation, small population size, low allelic diversity, and high levels of among-population differentiation suggest that repeated instances of founder events and genetic drift have been important in the evolution of this tropical shrub complex.     

Inferring ancient Agave cultivation practices from contemporary genetic patterns

Several Agave species have played an important ethnobotanical role since prehistory in Mesoamerica and semiarid areas to the north, including central Arizona. We examined genetic variation in relict Agave parryi populations northeast of the Mogollon Rim in Arizona, remnants from anthropogenic manipulation over 600 years ago. We used both allozymes and microsatellites to compare genetic variability and structure in anthropogenically manipulated populations with putative wild populations, to assess whether they were actively cultivated or the result of inadvertent manipulation, and to determine probable source locations for anthropogenic populations. Wild populations were more genetically diverse than anthropogenic populations, with greater expected heterozygosity, polymorphic loci, effective number of alleles and allelic richness. Anthropogenic populations exhibited many traits indicative of past active cultivation: fixed heterozygosity for several loci in all populations (nonexistent in wild populations); fewer multilocus genotypes, which differed by fewer alleles; and greater differentiation among populations than was characteristic of wild populations. Furthermore, manipulated populations date from a period when changes in the cultural context may have favoured active cultivation near dwellings. Patterns of genetic similarity among populations suggest a complex anthropogenic history. Anthropogenic populations were not simply derived from the closest wild A. parryi stock; instead they evidently came from more distant, often more diverse, wild populations, perhaps obtained through trade networks in existence at the time of cultivation.     

Population structure of red-cockaded woodpeckers in south Florida: RAPDs revisited

Six south Florida populations of the endangered red-cockaded woodpecker (Picoides borealis) were sampled to examine genetic diversity and population structure in the southernmost portion of the species' range relative to 14 previously sampled populations from throughout the species range. Random amplified polymorphic DNA (RAPD) analyses were used to evaluate the populations (n= 161 individuals, 13 primers, one band/primer). Results suggested that south Florida populations have significant among-population genetic differentiation (F_ST= 0.17, P < 0.000), although gene flow may be adequate to offset drift (N_m= 1.26). Comparison of Florida populations with others sampled indicated differentiation was less in Florida (F_ST for all populations = 0.21). Cluster analyses of all 20 populations did not reflect complete geographical predictions, although clustering of distant populations resulted in a significant correlation between genetic distance and geographical distance. Overall, results suggest populations in south Florida, similar to the remainder of the species, have low genetic diversity and high population fragmentation. Exact clustering of distant populations supports the ability of RAPDs to differentiate populations accurately. Our results further support past management recommendations that translocations of birds among geographically proximate populations is preferable to movement of birds between distant populations.     

Consistency of population genetics parameters estimated from isozyme and RAPDs dataset in species of genus <Emphasis Type="Italic">Prosopis</Emphasis> (Leguminosae,Mimosoideae)

Genetic variability, population structure and differentiation among 17 populations of 5 species and 2 natural interspecific hybrids of section Algarobia of genus Prosopis were analyzed from data of 23 isozyme and 28 RAPD loci. Both markers indicated that the studied populations are highly variable. P. alba populations in average showed lower values of genetic variability estimates from isozyme data, but this trend was not observed for RAPD markers. The hierarchical analyses of the distribution of genetic variability showed that the highest proportion of variation occurred within populations, the differentiation among species was intermediate and the lowest component was observed among populations within species. The consistency between results from both dataset implies that they are not biased and reflect the actual genetic structure of the populations analyzed. The matrices of Euclidean distances obtained from the two sets of markers were highly correlated according to Mantel test. In both cases the corresponding phenogram and MDS plot tended to cluster conspecific populations while hybrid populations were not intermediate between putative parents. Some disagreements between isozyme and RAPD phenograms were observed mainly in the affinities of hybrid populations. Such inconsistencies might result from reticular rather than dichotomic evolutionary relationships. The phenetic associations retrieved gave no support to the division of the section Algarobia into series.     

Genetic structure of wild bean populations in their South-Andean centre of origin

 The genetic structure of wild common bean populations was studied in the South-Andean centre of origin of the species. Plants were collected from 21 populations in Argentina and genetic variability was assessed for molecular and resistance markers. Polymorphism was weak for phaseolin, the major seed-storage protein, and for RAPD markers, while a high level of polymorphism was observed for resistance to anthracnose, one of the most important diseases of common bean. For the three traits, within-population variability was important and represented between 43.6% and 67.5% of the total variation. Although among-population differentiation was significant for all the traits, no correlation was found between the population distances calculated from RAPDs and resistance. These results indicate that pathogen selection pressure may be an important factor influencing the distribution of variability within and among host plant populations. Received: 28 October 1997 / Accepted: 25 November 1997     

Genetic differentiation among populations ofArabis serrata (Brassicaceae) along its geographic distribution

Levels and distribution of genetic variation were investigated in ten populations of the perennialArabis serrata distributed along a latitudinal gradient throughout Japan. Populations of this endemic species occupy predominantly three types of habitats: limestone and derived soils, volcanic and disturbed sites. Previous studies showed that plants ofA. serrata are differentiated in morphological and ecological traits under both natural conditions and common garden experiments suggesting genetic differentiation among populations. To assess the degree of genetic differentiation under different habitats ofA. serrata populations, we analyzed the isozyme genetic structure. Ten populations, located in mountains of central and northern Honshu and Hokkaido, were analyzed by starch gel enzyme electrophoresis. Fourteen loci of eight enzymes were resolved and six loci were monomorphic for all the populations. Populations sampled maintain low levels of genetic variation (P=0.16;H=0.05;A=1.16) compared to that maintained by other outcrossing seed plants. In some cases, few or no heterozygous individuals were detected, and consequently, mean observed heterozygosity was zero or near zero. Six (29%) of the fixation indices,F, estimated deviated significantly from Hardy Weinberg genotypic expectations indicating a deficiency of heterozygotes in most of the cases. The mean genetic identity (Nei'sI) between population pairs was 0.852 and indicates a moderate level of genetic differentiation among populations.Arabis serrata has most of its genetic variation distributed among rather than within populations. The among-population component of the total genetic diversity (G _ST mean value) was 0.416, indicating genetic differentiation between populations. There groups of populations were recognized in an unrooted tree generated by the Neighbor-Joining method. These results suggest groups of populations differentiated regionally. Estimates of interpopulational gene flow (Nm) were very variable (range 0.049–3.718) with a meanNm=1.203 for all populations.     

Genetic variability and reproductive effort in Polygonum pensylvanicum

Six populations of the annual plant Polygonum pensylvanicum were analysed for isozyme variability and reproductive effort. The populations were found to be similar in both their isozyme constituents and in their mean reproductive efforts. Mean reproductive effort did not correlate with mean population heterozygosity nor did individual reproductive effort correlate with individual heterozygosity. Polygonum pensylvanicum exhibits several of the features which have been predicted for weedy plant species.     

Influence of plant domestication on plant-pollinator interactions: Floral attributes and floral visitor communities in wild and cultivated squash plants

Premise

Domestication of plant species results in phenotypic modifications and changes in biotic interactions. Most studies have compared antagonistic plant-herbivore interactions of domesticated plants and their wild relatives, but little attention has been given to how domestication influences plant-pollinator interactions. Floral attributes and interactions of floral visitors were compared between sister taxa of the genus Cucurbita (Cucurbitaceae), the domesticated C. moschata, C. argyrosperma ssp. argyrosperma and its wild progenitor C. argyrosperma ssp. sororia in the place of origin.

Methods

We conducted univariate and multivariate analyses to compare floral morphological traits and analyzed floral reward (nectar and pollen) quantity and quality between flowers of wild and domesticated Cucurbita taxa. Staminate and pistillate flowers of all three taxa were video recorded, and visitation and behavior of floral visitors were registered and analyzed.

Results

Most floral morphological characteristics of flowers of domesticated taxa were larger in both staminate and pistillate flowers. Staminate and pistillate flowers presented distinct correlations between floral traits and integration indices between domesticated and wild species. Additionally, pollen quantity and protein to lipid ratio were greater in domesticated species. Cucurbit pollen specialists, Eucera spp., had the highest probability of visit for all Cucurbita taxa.

Conclusions

We provide evidence that floral traits of domesticated and wild Cucurbita species experienced different selection pressures. Domesticated Cucurbita species may have more resources invested towards floral traits, thereby increasing attractiveness to pollinators and potentially plant reproductive success. Wild ancestor plant populations should be conserved in their centers of origin to preserve plant-pollinator interactions.     

Evolutionary potential in the wild: more than meets the eye

The genus Aquilegia consists of 60–70 perennial plant species widely distributed throughout the northern hemisphere. Its flowers have a delicate and ornamental appearance that makes them a favourite of gardeners. In this genus, adaptive radiations for both floral and vegetative traits have occurred. These adaptive radiations, and the key phylogenetic placement of Aquilegia between Arabidopsis and rice, make this genus a ‘model system’ for plant evolution ( Kramer 2009 ). In this issue, Castellanos et al. (2011) use a marker‐based method to infer heritability for floral and vegetative traits in two Aquilegia species. Layered on top of this are estimates of the strength of natural selection. This novel joint estimation of heritability and selection in the wild showed that vegetative traits, compared to floral traits, have the highest evolutionarily potential. Evolutionary potential is the most important quantity to measure in wild populations. It combines inheritance and strength of selection and predicts the potential for populations to adapt to changing environments. The combination of molecular techniques with species in natural environments makes this work a model for molecular ecological investigations.     

Comparison of quantitative and molecular variation in agroforestry populations of the shea tree (Vitellaria paradoxa C.F. Gaertn) in Mali

In this study we investigated the within- and between-population genetic variation using microsatellite markers and quantitative traits of the shea tree, Vitellaria paradoxa, an important agroforestry tree species of the Sudano–Sahelian region in Africa. Eleven populations were sampled across Mali and in northern Côte d’Ivoire. Leaf size and form and growth traits were measured in a progeny test at the nursery stage. Eight microsatellites were used to assess neutral genetic variation. Low levels of heterozygosity were recorded (1.6–3.0 alleles/locus; H_E = 0.25–0.42) and the fixation index (F_IS = −0.227–0.186) was not significantly different from zero suggesting that Hardy–Weinberg equilibrium is encountered in all populations sampled. Quantitative traits exhibited a strong genetic variation between populations and between families within populations. The degree of population differentiation of the quantitative traits (Q_ST = 0.055–0.283, Q_STmean = 0.189) strongly exceeds that in eight microsatellite loci (F_ST = −0.011–0.142, F_STmean = 0.047). Global and pairwise F_ST values were very low and not significantly different from zero suggesting agroforestry practices are amplifying gene flow (Nm = 5.07). The population means for quantitative traits and the rainfall variable were not correlated, showing variation was not linked with this climatic cline. It is suggested that this marked differentiation for quantitative traits, independent of environmental clines and despite a high gene flow, is a result of local adaptation and human selection of shea trees. This process has induced high linkage disequilibrium between underlying loci of polygenic characters.     

Genetic Differentiation of Pedunculate Oak Quercus robur L. in the European Part of Russia Based on RAPD Markers

Using randomly amplified polymorphic DNA markers (RAPD), genetic variation and differentiation in four populations of pedunculate oak Quercus robur L. were examined. The populations occupy a large part of the Quercus robur range in the European Russia (Voronezh and Novgorod oblasts; Republics of Mordovia and Bashkortostan). With each of six random primers (A02, A09, A17, B01, B08, B11), 96 DNA samples were analyzed by PCR. In all, 48 putative polymorphic RAPD loci were detected. We failed to reveal population-specific DNA fragments for any primer although the frequencies of 14 fragments were significantly different among populations. The oak populations studied exhibited high variability: 73–90% of genes were polymorphic and the effective allele number was about 1.4. The total genetic variation varied from 0.202 (Vor) to 0.245 (Nov), which corresponded to the estimates for populations of this species from Central and Western Europe. The populations examined showed low among-population differentiation (G _ST = 0.098); gene flow N _e m was 4.61. The proportion of among-population variation of the RAPD loci studied accounted for 7% of the total variability; more than 93% of the total variability was explained by individual and within-population variation.     

Genetic diversity and local population structure in Ambrosina bassii (Araceae,Ambrosineae), a Mediterranean relict species

The effects of habitat fragmentation on the genetic structure of Ambrosina bassii are analyzed. The species, whose reproductive biology is mostly unknown, is the only representative of its genus and tribe and it is endemic to the central Mediterranean area. The selected study area was the island of Sicily, in which wild populations show a wide morphological variability and ecological amplitude. Patterns of within- and among-population genetic diversity in eleven Sicilian populations, occurring in six disjunct areas, were examined by means of allozyme electrophoresis. High levels of genetic diversity were found as shown by the mean expected heterozygosity (H_e = 0.263), the percentage of polymorphic loci (P₉₅ = 65.3), the mean number of alleles per locus (A = 2.0). Genetic differentiation between populations was relatively low (mean F_ST = 0.091 and Nm = 1.98). A very weak correlation exists between genetic distances and geographic distances between populations. Despite its restricted and fragmented geographical range, A. bassii showed (i) high levels of genetic diversity, mainly within populations; (ii) no genetic differentiation between populations and morphotypes.     

Phenotypic integration and the potential for independent color evolution in a polymorphic spring ephemeral

The genetic architecture of the total phenotype may substantially constrain or enhance the evolution of floral color within populations in response to multiple selection pressures. Using Claytonia virginica I previously identified opposing selection on floral color generated through herbivores and pathogens. Here I ask whether the evolution of floral color in this system is constrained or unconstrained by its phenotypic integration with floral and vegetative traits. Morphological, physiological, and pollen traits were measured on over 400 plants in the field and greenhouse, and these data were used to test whether floral-color morphs differed with respect to other traits and whether the among-trait correlation structure differed across the color morphs. The color morphs varied with respect to most measured traits; however, the pattern of variation was not consistent among them, and there was little evidence of trade-offs with floral color. A common principal components analysis revealed that the pattern of phenotypic integration substantially differed among the color morphs. Combined, these results suggest that floral-color evolution may proceed relatively unconstrained by associations with other traits in this system. The absence of a strong constraint in combination with known fluctuating selective pressures may help to explain observed within- and among-population color variation in this species.