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.     

Intra-population comparison of vegetative and floral trait heritabilities estimated from molecular markers in wild Aquilegia populations

Measuring heritable genetic variation is important for understanding patterns of trait evolution in wild populations, and yet studies of quantitative genetic parameters estimated directly in the field are limited by logistic constraints, such as the difficulties of inferring relatedness among individuals in the wild. Marker-based approaches have received attention because they can potentially be applied directly to wild populations. For long-lived, self-compatible plant species where pedigrees are inadequate, the regression-based method proposed by Ritland has the appeal of estimating heritabilities from marker-based estimates of relatedness. The method has been difficult to implement in some plant populations, however, because it requires significant variance in relatedness across the population. Here, we show that the method can be readily applied to compare the ability of different traits to respond to selection, within populations. For several taxa of the perennial herb genus Aquilegia, we estimated heritabilities of floral and vegetative traits and, combined with estimates of natural selection, compared the ability to respond to selection of both types of traits under current conditions. The intra-population comparisons showed that vegetative traits have a higher potential for evolution, because although they are as heritable as floral traits, selection on them is stronger. These patterns of potential evolution are consistent with macroevolutionary trends in the European lineage of the genus.     

Genetic constraints on phenotypic evolution in Nigella (Ranunculaceae)

The present investigation examines the role of genetic constraints in shaping evolutionary change in the Nigella arvensis species complex. Parent-offspring analyses of two populations of N. degenii demonstrated high heritabilities for a wide range of vegetative and floral characters, indicating a great potential for further adaptive change. The populations differed significantly in the heritability for leaf length and in the genetic correlation between plant height and peduncle length, suggesting that these populations would respond differently to identical selection pressures. There was a tendency for large-scale diversity to extrapolate within-population variability, at least for the floral trait associations, while genetic data from a segregating F3 hybrid population indicated stability in the correlation structure across two environments. On the basis of hybrid data, I propose that inbreeding effects and pleiotropic relationships with leaf size may have facilitated the reduction in floral morphology accompanying the evolution of autogamy in related taxa.     

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.     

Morphological variation pattern of Aquilegia ecalcarata and its relatives

Aquilegia ecalcarata Maxim. is the only spurless species within the genus Aquilegia and comprises a monophyletic clade with A. yabeana Kitag., A. kansuensis Brühl, and A. rockii Munz. Our previous study on the genetic diversity of those four species revealed that the populations of A. ecalcarata can be divided into two groups, indicating possible genetic difference within A. ecalcarata. However, it is not clear whether the genetic difference is related to the morphological variation among species and groups of A. ecalcarata populations. To answer that question, the morphological variation patterns based on 22 floral and 19 vegetative traits from 42 populations, covering the entire distribution of A. ecalcarata and its relatives, were analyzed in the present study. The result showed that: (i) the differences among the four species were reflected in the floral rather than the vegetative traits; (ii) populations of A. yabeana and A. rockii fell into one cluster each, and each of the six clusters occupied its own distribution range; (iii) one of two A. ecalcarata clusters fell into a subgroup and shared common floral traits with A. rockii; (iv) the individuals of A. ecalcarata form. ecalcarata and form. semicalcarata were often mixed in the same population; and (v) the populations of A. kansuensis were split into two clusters, which differed obviously in floral traits. These results will provide an important morphological basis for the redefinition of species and lay a foundation for the further exploration of the “spurless” A. ecalcarata.     

Divergent selection on flowering phenology but not on floral morphology between two closely related orchids

Closely related species often differ in traits that influence reproductive success, suggesting that divergent selection on such traits contribute to the maintenance of species boundaries. Gymnadenia conopsea ss. and Gymnadenia densiflora are two closely related, perennial orchid species that differ in (a) floral traits important for pollination, including flowering phenology, floral display, and spur length, and (b) dominant pollinators. If plant–pollinator interactions contribute to the maintenance of trait differences between these two taxa, we expect current divergent selection on flowering phenology and floral morphology between the two species. We quantified phenotypic selection via female fitness in one year on flowering start, three floral display traits (plant height, number of flowers, and corolla size) and spur length, in six populations of G. conopsea s.s. and in four populations of G. densiflora. There was indication of divergent selection on flowering start in the expected direction, with selection for earlier flowering in two populations of the early‐flowering G. conopsea s.s. and for later flowering in one population of the late‐flowering G. densiflora. No divergent selection on floral morphology was detected, and there was no significant stabilizing selection on any trait in the two species. The results suggest ongoing adaptive differentiation of flowering phenology, strengthening this premating reproductive barrier between the two species. Synthesis: This study is among the first to test whether divergent selection on floral traits contribute to the maintenance of species differences between closely related plants. Phenological isolation confers a substantial potential for reproductive isolation, and divergent selection on flowering time can thus greatly influence reproductive isolation and adaptive differentiation.     

Can indirect selection and genetic context contribute to trait diversification? A transition‐probability study of blossom‐colour evolution in two genera

Darwin recognized that biological diversity has accumulated as a result of both adaptive and nonadaptive processes. Very few studies, however, have addressed explicitly the contribution of nonadaptive processes to evolutionary diversification, and no general procedures have been established for distinguishing between adaptive and nonadaptive processes as sources of trait diversity. I use the diversification of flower colour as a model system for attempting to identify adaptive and nonadaptive causes of trait diversification. It is widely accepted that variation in flower colour reflects direct, adaptive response to divergent selective pressures generated by different pollinators. However, diversification of flower colour may also result from the effects of nonadaptive, pleiotropic relationships with vegetative traits. Floral pigments that have pleiotropic relationships to vegetative pigments may evolve and diversify in at least two nonadaptive ways. (1) Indirect response to selection on the pleiotropically related nonfloral traits may occur (indirect selection). (2) Divergent evolution in response to parallel selective pressures (e.g. selection by pollinators for visually obvious flowers) may occur because populations are at different genetic starting points, and each population follows its own genetic `line of least resistance.' A survey of literature suggests that pleiotropic relationships between flower colour and vegetative traits are common. Phylogenetically informed analyses of comparative data from Dalechampia (Euphorbiaceae) and Acer (Aceraceae), based on trait‐transition probabilities and maximum likelihood, indicated that floral and vegetative pigments are probably pleiotropically related in these genera, and this relationship better explains the diversification of floral colour than does direct selection by pollinators. In Dalechampia pink/purple floral bract colour may have originated by indirect response to selection on stem and leaf pigments. In Acer selection by pollinators for visually obvious flowers may to have led to the evolution of red or purple flowers in lineages synthesizing and deploying red anthocyanins in leaves, and pale‐green or yellow flowers in species not deploying red anthocyanins in vegetative structures. This study illustrates the broader potential of indirect selection and parallel selection on different genetic starting points to contribute to biological diversity, and the value of testing directly for the operation of these nonadaptive diversifying processes.     

Strong conservatism of floral morphology during the rapid diversification of the genus Helianthemum

Premise

Divergence of floral morphology and breeding systems are often expected to be linked to angiosperm diversification and environmental niche divergence. However, available evidence for such relationships is not generalizable due to different taxonomic, geographical and time scales. The Palearctic genus Helianthemum shows the highest diversity of the family Cistaceae in terms of breeding systems, floral traits, and environmental conditions as a result of three recent evolutionary radiations since the Late Miocene. Here, we investigated the tempo and mode of evolution of floral morphology in the genus and its link with species diversification and environmental niche divergence.

Methods

We quantified 18 floral traits from 83 taxa and applied phylogenetic comparative methods using a robust phylogenetic framework based on genotyping-by-sequencing data.

Results

We found three different floral morphologies, putatively related to three different breeding systems: type I, characterized by small flowers without herkogamy and low pollen to ovule ratio; type II, represented by large flowers with approach herkogamy and intermediate pollen to ovule ratio; and type III, featured by small flowers with reverse herkogamy and the highest pollen to ovule ratio. Each morphology has been highly conserved across each radiation and has evolved independently of species diversification and ecological niche divergence.

Conclusions

The combined results of trait, niche, and species diversification ultimately recovered a pattern of potentially non-adaptive radiations in Helianthemum and highlight the idea that evolutionary radiations can be decoupled from floral morphology evolution even in lineages that diversified in heterogeneous environments as the Mediterranean Basin.     

贵州特有药用植物毕节小檗的形态变异

为探讨贵州特有药用植物毕节小檗(Berberis guizhouensis)形态多样性的变异式样及其适应机制,对其野外居群营养器官和花部形态进行研究。对毕节小檗一直空缺的花部性状进行了描述。结果表明,毕节小檗的性状在同一居群或同一性状在不同居群中都存在较丰富的变异,变异系数为0.03~0.57。从总体来看,营养器官性状的变异程度要高于花部性状。单因素方差分析表明居群间部分花部性状存在显著差异(P0.05)。聚类分析表明小白岩居群形成1个独立的分支,这种分化很可能是环境压力选择的结果。主成分分析表明花部性状与营养性状在维持形态结构的稳定性具有协调一致的生态适应。     

Linking divergent selection on vegetative traits to environmental variation and phenotypic diversification in the Iberian columbines (Aquilegia)

Divergent selection is a key in the ecological theory of adaptive radiation. Most evidence on its causes and consequences relies on studies of pairs of populations or closely related taxa. However, adaptive radiation involves multiple taxa adapted to different environmental factors. We propose an operational definition of divergent selection to explore the continuum between divergent and convergent selection in multiple populations and taxa, and its links with environmental variation and phenotypic and taxonomic differentiation. We apply this approach to explore phenotypic differentiation of vegetative traits between 15 populations of four taxa of Iberian columbines (Gen. Aquilegia). Differences in soil rockiness impose divergent selection on inflorescence height and the number of flowers per inflorescence, likely affecting the processes of phenotypic and, in the case of inflorescence height, taxonomic diversification between taxa. Elevational variation imposes divergent selection on the number of leaves; however, the current pattern of divergent selection on this trait seems related to ecotypic differentiation within taxa but not to their taxonomic diversification.     

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.     

Adaptive genetic differentiation in life-history traits between populations of <Emphasis Type="Italic">Mimulus guttatus</Emphasis> with annual and perennial life-cycles

The optimal allocation to sexual and vegetative reproduction as well as the optimal values of other life-history characteristics such as phenology, growth and mating system are likely to depend on the life-cycle of the organism. I tested whether plants of Mimulus guttatus originating from temporarily wet populations where the species has an enforced annual life-cycle have higher allocation to sexual reproduction, lower allocation to vegetative reproduction, more rapid phenology, faster growth, and floral traits associated with a self-fertilizing mating system than plants from permanently wet populations where the species has a perennial life-cycle. I grew a total of 1377 plants originating from three populations with an annual life-cycle and 11 populations with a perennial life-cycle in a greenhouse under permanently and temporarily wet conditions. Plants of M. guttatus in permanently wet conditions had significantly more vegetative reproduction and tended to have a faster growth than plants in the temporarily wet conditions, indicating plasticity in these life-history traits. Plants from populations with an annual life-cycle invested significantly more in sexual reproduction and significantly less in vegetative reproduction than the ones from populations with a perennial life-cycle. Moreover, this study showed that plants originating from populations with an annual life-cycle have a significantly faster development and floral traits associated with autonomous self-fertilization. In conclusion, this study suggests that there has been adaptive evolution of life history traits of M. guttatus in response to natural watering conditions that determine the life span of the species.     

Patterns of genetic variability within and among populations of wild radish,Raphanus raphanistrum (Brassicaceae)

The genetic structure of populations is an important determinant of the evolutionary potential of a species. Colonizing plants tend to be characterized by low within- and high among-population variability. Genetic differentiation of both floral traits and isozymes was studied in six populations of wild radish (Raphanus raphanistrum). Evidence for differentiation in both sets of traits was found, but patterns of differentiation of floral traits did not coincide with isozyme differentiation. Contrary to most colonizing species, wild radish showed high within- and only moderate among-population variability at isozyme loci. In addition, levels of differentiation did not correspond to geographic distance between the populations. These results are likely due at least in part to the self-incompatibility system of this species, long-distance movement of large numbers of wild radish seeds by humans, and introgression from cultivated radish (R. sativus).     

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.     

Floral traits and isolation of three sympatric Aquilegia species in the Qinling Mountains, China

Floral isolation has been considered to be an important reproductive mechanism governing the species diversification in many genera. In a classic example Aquilegia, sympatric species from North America with diverse floral traits are generally associated with specialized pollinators that prohibit interspecific hybridization. It remains unclear whether species diversification in the genus from Eurasia is also maintained by floral isolation. We investigated floral phenology, floral characteristics and pollinators in three sympatric Aquilegia species (A. ecalcarata, A. incurvata and A. yabeana) in the Qinling Mountains, Shanxi Province, China from 2001 to 2005. The spurless A. ecalcarata flowers earlier than the other two species with nectar spurs but their floral phenology overlaps. Major pollinators of A. ecalcarata are syrphid flies while bumblebees are major for A. incurvata and A. yabeana. Therefore our observations confirm that mechanical isolation through differential pollinators could contribute reproductive isolation between spurless and spurred species, as demonstrated by studies from North America. Whether floral isolation plays a major role in the reproductive isolation between two spurred species (A. incurvata and A. yabeana), however, remains to be seen. Further studies are required to quantify the potential role of geographical isolation because they occupy different habitats.     

Colonization history and genetic diversity: adaptive potential in early stage invasions

The introduction of Anolis cristatellus from the multiple species anole community of Puerto Rico in the Greater Antilles to the island of Dominica in the Lesser Antilles, with its solitary endemic anole, provides an example of a very recent, timed, single colonization. We investigate the geographic origin and adaptive potential of the Dominican population using a range of methods including mtDNA phylogeography, nuclear microsatellite variation and multiple paternity studies, as well as heritability estimates, common garden experiments and comparative geographic studies of quantitative scalation traits. Phylogeographic analysis of NADH2 and microsatellite studies suggests that the Dominican population arose from a set of individuals from the central west area of Puerto Rico within their endemic range. The multiple‐individual inoculation, together with sperm storage and evidence of multiple paternity indicate genetic variability and suggest the potential for adaptation by natural selection. Estimates of heritability, common garden experiments and broad sense Q_ST/F_ST ratios, linked to replicated comparisons along elevational transects go some way to suggesting that the invasive populations may be adapting by natural selection, in parallel with the endemic anole, in the brief period since their introduction.     

Environmental stress correlates with increases in both genetic and residual variances: A meta‐analysis of animal studies

Adaptive evolutionary responses are determined by the strength of selection and amount of genetic variation within traits, however, both are known to vary across environmental conditions. As selection is generally expected to be strongest under stressful conditions, understanding how the expression of genetic variation changes across stressful and benign environmental conditions is crucial for predicting the rate of adaptive change. Although theory generally predicts increased genetic variation under stress, previous syntheses of the field have found limited support for this notion. These studies have focused on heritability, which is dependent on other environmentally sensitive, but nongenetic, sources of variation. Here, we aim to complement these studies with a meta‐analysis in which we examine changes in coefficient of variation (CV) in maternal, genetic, and residual variances across stressful and benign conditions. Confirming previous analyses, we did not find any clear direction in how heritability changes across stressful and benign conditions. However, when analyzing CV, we found higher genetic and residual variance under highly stressful conditions in life‐history traits but not in morphological traits. Our findings are of broad significance to contemporary evolution suggesting that rapid evolutionary adaptive response may be mediated by increased evolutionary potential in stressed populations.     

Heritability and genetic correlations of personality traits in a wild population of yellow‐bellied marmots (Marmota flaviventris)

Describing and quantifying animal personality is now an integral part of behavioural studies because individually distinctive behaviours have ecological and evolutionary consequences. Yet, to fully understand how personality traits may respond to selection, one must understand the underlying heritability and genetic correlations between traits. Previous studies have reported a moderate degree of heritability of personality traits, but few of these studies have either been conducted in the wild or estimated the genetic correlations between personality traits. Estimating the additive genetic variance and covariance in the wild is crucial to understand the evolutionary potential of behavioural traits. Enhanced environmental variation could reduce heritability and genetic correlations, thus leading to different evolutionary predictions. We estimated the additive genetic variance and covariance of docility in the trap, sociability (mirror image stimulation), and exploration and activity in two different contexts (open‐field and mirror image simulation experiments) in a wild population of yellow‐bellied marmots (Marmota flaviventris). We estimated both heritability of behaviours and of personality traits and found nonzero additive genetic variance in these traits. We also found nonzero maternal, permanent environment and year effects. Finally, we found four phenotypic correlations between traits, and one positive genetic correlation between activity in the open‐field test and sociability. We also found permanent environment correlations between activity in both tests and docility and exploration in the MIS test. This is one of a handful of studies to adopt a quantitative genetic approach to explain variation in personality traits in the wild and, thus, provides important insights into the potential variance available for selection.     

Selection at behavioural,developmental and metabolic genes is associated with the northward expansion of a successful tropical colonizer

What makes a species able to colonize novel environments? This question is key to understand the dynamics of adaptive radiations and ecological niche shifts, but the mechanisms that underlie expansion into novel habitats remain poorly understood at a genomic scale. Lizards from the genus Anolis are typically tropical, and the green anole (Anolis carolinensis) constitutes an exception since it expanded into temperate North America from subtropical Florida. Thus, we used the green anole as a model to investigate signatures of selection associated with colonization of a new environment, namely temperate North America. To this end, we analysed 29 whole‐genome sequences, covering the entire native range of the species. We used a combination of recent methods to quantify both positive and balancing selection in northern populations, including F_ST outlier methods, machine learning and ancestral recombination graphs. We naively scanned for genes of interest and assessed the overlap between multiple tests. Strikingly, we identified many genes involved in behaviour, suggesting that the recent successful colonization of northern environments may have been linked to behavioural shifts as well as physiological adaptation. Using a candidate genes strategy, we determined that genes involved in response to cold or behaviour displayed more frequently signals of selection, while controlling for local recombination rate, gene clustering and gene length. In addition, we found signatures of balancing selection at immune genes in all investigated genetic groups, but also at genes involved in neuronal and anatomical development.