Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: evidence for modular genetic architecture

Summary Morphological variation within organisms is integrated and often modular in nature. That is to say, the size and shape of traits tend to vary in a coordinated and structured manner across sets of organs or parts of an organism. The genetic basis of this morphological integration is largely unknown. Here, we report on quantitative trait loci (QTL) analysis of leaf and floral organ size in Arabidopsis thaliana. We evaluate patterns of genetic correlations among traits and perform whole-genome scans using QTL mapping methods. We detected significant genetic variation for the size and shape of each floral and leaf trait in our study. Moreover, we found large positive genetic correlations among sets of either flower or leaf traits, but low and generally nonsignificant genetic correlations between flower and leaf traits. These results support the hypothesis of independent floral and vegetative modules. We consider co-localization of QTL for different traits as support for a pleiotropic basis of morphological integration and modularity. A total of eight QTL affecting flower and three QTL affecting leaf traits were identified. Most QTL affected either floral or leaf traits, providing a general explanation for high correlations within and low correlations between modules. Only two genomic locations affected both flower and leaf growth. These results are discussed in the context of the evolution of modules, pleiotropy, and the putative homologous relationship between leaves and flowers.     

Genetic architecture,biochemical underpinnings and ecological impact of floral UV patterning

Floral attraction traits can significantly affect pollinator visitation patterns, but adaptive evolution of these traits may be constrained by correlations with other traits. In some cases, molecular pathways contributing to floral attraction are well characterized, offering the opportunity to explore loci potentially underlying variation among individuals. Here, we quantify the range of variation in floral UV patterning (i.e. UV ‘bulls‐eye nectar guides) among crop and wild accessions of Brassica rapa. We then use experimental crosses to examine the genetic architecture, candidate loci and biochemical underpinnings of this patterning as well as phenotypic manipulations to test the ecological impact. We find qualitative variation in UV patterning between wild (commonly lacking UV patterns) and crop (commonly exhibiting UV patterns) accessions. Similar to the majority of crops, recombinant inbred lines (RILs) derived from an oilseed crop × WI fast‐plant^® cross exhibit UV patterns, the size of which varies extensively among genotypes. In RILs, we further observe strong statistical‐genetic and QTL correlations within petal morphological traits and within measurements of petal UV patterning; however, correlations between morphology and UV patterning are weak or nonsignificant, suggesting that UV patterning is regulated and may evolve independently of overall petal size. HPLC analyses reveal a high concentration of sinapoyl glucose in UV‐absorbing petal regions, which, in concert with physical locations of UV‐trait QTLs, suggest a regulatory and structural gene as candidates underlying observed quantitative variation. Finally, insects prefer flowers with UV bulls‐eye patterns over those that lack patterns, validating the importance of UV patterning in pollen‐limited populations of B. rapa.     

Identification of Selection Signatures in Cattle Breeds Selected for Dairy Production

Genetic correlations are expected to be high among functionally related traits and lower between groups of traits with distinct functions (e.g., reproductive vs. resource-acquisition traits). Here, we explore the quantitative-genetic and QTL architecture of floral organ sizes, vegetative traits, and life history in a set of Brassica rapa recombinant inbred lines within and across field and greenhouse environments. Floral organ lengths were strongly positively correlated within both environments, and analysis of standardized G-matrices indicates that the structure of genetic correlations is ∼80% conserved across environments. Consistent with these correlations, we detected a total of 19 and 21 additive-effect floral QTL in the field and the greenhouse, respectively, and individual QTL typically affected multiple organ types. Interestingly, QTL × QTL epistasis also appeared to contribute to observed genetic correlations; i.e., interactions between two QTL had similar effects on filament length and two estimates of petal size. Although floral and nonfloral traits are hypothesized to be genetically decoupled, correlations between floral organ size and both vegetative and life-history traits were highly significant in the greenhouse; G-matrices of floral and vegetative traits as well as floral and life-history traits differed across environments. Correspondingly, many QTL (45% of those mapped in the greenhouse) showed environmental interactions, including approximately even numbers of floral and nonfloral QTL. Most instances of QTL × QTL epistasis for floral traits were environment dependent.EVOLUTIONARY responses to selection are dependent on genetic architecture. The proportion of phenotypic variation with a heritable genetic basis affects the response to selection, as does the structure of genetic correlations among selected traits. For example, an evolutionary response will be constrained if selection favors an increase in the value of two traits that are negatively correlated; i.e., a negative correlation is antagonistic to the joint vector of selection. Alternatively, if the vector of selection is parallel to the genetic correlation, then trait covariation is reinforcing and the population mean may more rapidly approach favored trait values (Etterson and Shaw 2001; Merilä and Björklund 2004). One measure of genetic architecture is the G-matrix (Lynch and Walsh 1998), which is composed of genetic variances (diagonal matrix elements) and genetic covariances among traits (off-diagonal matrix elements). G-matrices have been shown to vary across environments (Donohue et al. 2000; Conner et al. 2003; Brock and Weinig 2007), indicating that the molecular-genetic underpinnings of matrix elements (e.g., identity and/or relative effect of additive and epistatic loci, degree of pleiotropy, etc.) and the traits'' evolutionary potential vary across environments. Few studies, however, have related matrix and QTL architectures; and, therefore, the molecular-genetic underpinnings of quantitative-genetic estimates remain unclear (but see Gardner and Latta 2007; Kelly 2009).In angiosperms, covariances between floral whorls (e.g., petal and stamen length) are frequently positive among functionally related traits. These positive correlations can arise from pollinator-mediated (or pollination-mediated) selection for specific allometric relationships among floral traits and ensuing linkage disequilibrium (LD) among causal loci (Berg 1959, 1960; also referred to as phenotypic integration, see Pigliucci 2003; Klingenberg 2008). For example, in outcrossing species, male fitness may be more dependent on the frequency and efficiency of pollinator visitation than female fitness (Bell 1985; but see Hodgins and Barrett 2008). Anther placement relative to the corolla opening can affect the efficiency of pollen dissemination (Conner and Via 1993; Morgan and Conner 2001); in addition, comparative work indicates that petal–stamen length correlations are stronger than stamen–pistil length correlations in outcrossers, whereas species that reproduce via autogamous selfing show the opposite pattern (Ushimaru and Nakata 2002). Alternatively, strong floral integration could be attributed to the developmental hypothesis that genetic correlations arise due to pleiotropic genes coregulating floral whorls (Herrera 2001; Herrera et al. 2002). Strong correlations resulting from linkage disequilibrium or from developmentally based pleiotropy may constrain the evolution of novel reproductive morphologies when biotic or abiotic factors (and selection) change (Cheverud 1984; Clark 1987; Smith and Rausher 2008; Agrawal and Stinchcombe 2009).Similar to genetic covariances among floral traits, covariances between floral and nonfloral traits could also alter the evolutionary response of reproductive traits. In contrast to hypotheses regarding the adaptive significance of floral-trait integration, genetic correlations between floral and nonfloral traits (e.g., vegetative or phenological traits) are hypothesized to be disadvantageous (Berg 1960). More specifically, floral allometry may be shaped by selection for reproductive success, as described above, whereas vegetative morphology is shaped primarily by selection to optimize other functions, such as light capture. If floral and nonfloral traits have a common genetic basis, then selection on phenological or morphological traits may result in maladaptive expression of floral organ size. As a result, functionally integrated floral traits are predicted to be genetically decoupled from vegetative and phenological traits (Berg 1960).QTL mapping provides a powerful tool to explore the genetic architecture of evolutionarily important traits. The QTL architecture of interspecific floral traits has been explored in diverse systems (Bradshaw et al. 1995; Fishman et al. 2002; Goodwillie et al. 2006; Bouck et al. 2007; Moyle 2007); however, insight into the molecular genetic basis of intraspecific floral variation comes almost exclusively from Arabidopsis thaliana (Juenger et al. 2000, 2005) and Mimulus guttatus (Hall et al. 2006). Floral traits in these intraspecific crosses are polygenic with a majority of detected QTL being of small to moderate effect size. Consistent with other quantitative-genetic studies (reviewed in Ashman and Majetic 2006), floral traits in A. thaliana and M. guttatus mapping populations exhibited moderate to high genetic correlations. In both systems, mapped QTL often affected multiple floral traits. In the few cases where QTL underlying intraspecific floral morphology have been evaluated, only a single growth environment was used; estimation of floral quantitative genetics across environments and subsequent comparison with the QTL architecture underlying observed across-environment patterns are lacking.Using a segregating progeny of Brassica rapa (recombinant inbred lines, RILs) and a small sample of crop and wild accessions, we examine the quantitative-genetic and QTL architecture of floral traits under field and greenhouse environments. Specifically, we address the following questions: (1) Does this RIL population express significant genetic (co)variation for floral traits when growing in the field or greenhouse? (2) Is there significant genetic variation for vegetative traits and days to flowering in field and greenhouse environments, and is there evidence for genetic correlations between floral and nonfloral traits? (3) Does the genetic architecture of floral and nonfloral traits, as measured by the G-matrix, differ across environments? (4) What is the number and effect size of additive and epistatic QTL in field and greenhouse environments? (5) What is the relationship between mapped QTL and quantitative genetic estimates of trait (co)variation within and between floral and nonfloral traits? And (6) what is the relationship between the quantitative-genetic architecture of floral traits in the RILs vs. in the accessions?     

The Influence of Modularity on Cranial Morphological Disparity in Carnivora and Primates (Mammalia)

Background

Although variation provides the raw material for natural selection and evolution, few empirical data exist about the factors controlling morphological variation. Because developmental constraints on variation are expected to act by influencing trait correlations, studies of modularity offer promising approaches that quantify and summarize patterns of trait relationships. Modules, highly-correlated and semi-autonomous sets of traits, are observed at many levels of biological organization, from genes to colonies. The evolutionary significance of modularity is considerable, with potential effects including constraining the variation of individual traits, circumventing pleiotropy and canalization, and facilitating the transformation of functional structures. Despite these important consequences, there has been little empirical study of how modularity influences morphological evolution on a macroevolutionary scale. Here, we conduct the first morphometric analysis of modularity and disparity in two clades of placental mammals, Primates and Carnivora, and test if trait integration within modules constrains or facilitates morphological evolution.

Principal Findings

We used both randomization methods and direct comparisons of landmark variance to compare disparity in the six cranial modules identified in previous studies. The cranial base, a highly-integrated module, showed significantly low disparity in Primates and low landmark variance in both Primates and Carnivora. The vault, zygomatic-pterygoid and orbit modules, characterized by low trait integration, displayed significantly high disparity within Carnivora. 14 of 24 results from analyses of disparity show no significant relationship between module integration and morphological disparity. Of the ten significant or marginally significant results, eight support the hypothesis that integration within modules constrains morphological evolution in the placental skull. Only the molar module, a highly-integrated and functionally important module, showed significantly high disparity in Carnivora, in support of the facilitation hypothesis.

Conclusions

This analysis of within-module disparity suggested that strong integration of traits had little influence on morphological evolution over large time scales. However, where significant results were found, the primary effect of strong integration of traits was to constrain morphological variation. Thus, within Primates and Carnivora, there was some support for the hypothesis that integration of traits within cranial modules limits morphological evolution, presumably by limiting the variation of individual traits.     

Phenotypic Integration Without Modularity: Testing Hypotheses About the Distribution of Pleiotropic Quantitative Trait Loci in a Continuous Space

Theories of phenotypic integration have relied heavily on the concept of modularity in order to model the ways in which traits in an organism correlate and covary. Recent investigations suggest that, while some functional and developmental processes may be morphologically and ontogenetically localized, and thus modular in a developmental sense, there is a great deal of overlap among these influences on patterns of integration in the adult form. This can result in blurry boundaries between hypothesized modules constructed to test hypotheses about phenotypic integration. This investigation tests hypotheses about the contribution of pleiotropic quantitative trait loci (QTL) to phenotypic integration in the mouse mandible without using a priori categorical hypotheses about which traits constitute a module. We ask two main questions: (1) Are the effects of pleiotropic QTL localized to highly correlated traits or more spread out among traits than one might expect by chance? (2) Does the pattern of trait influence when all pleiotropic QTL are considered together deviate from what we might expect if QTL affect traits without regard for the correlations among traits? We find that a large proportion of pleiotropic QTL affect traits that are more highly correlated than we expect by chance with the remainder having effects that are distributed as if by chance. Furthermore, the overall distribution of the effects of pleiotropic QTL differs significantly from the null distribution of no association between pleiotropic effects on traits and correlations among traits. The main modular hypothesis used by earlier studies often does not predict the distribution of sets of traits sharing a common QTL. These results suggest that there is a clear tendency for pleiotropic effects of QTL to be localized but that the localization may be best thought of as occurring in a continuous space rather being clustered in discrete modules.     

Plasticity and environment-specific covariances: an investigation of floral-vegetative and within flower correlations

Floral traits are commonly thought to be more canalized than vegetative ones. In addition, floral and vegetative traits are hypothesized to be genetically decoupled, enabling vegetative structures to respond plastically to environmental heterogeneity, and to evolve in response to selection without disrupting the reproductive function of flowers. To test these hypotheses, we evaluate the genetic architecture of floral and vegetative traits in natural populations of Arabidopsis thaliana raised under variable light-quality environments. Plants were grown either under high or low ratios of red to far-red (R:FR) light, an aspect of light quality that varies with neighbor proximity and regulates competitive shade-avoidance responses. Across environments, we detected significant genetic variation for the average expression of all measured floral traits (petal length and width, stamen length, pistil length, stigma-anther separation, and exsertion of both the stamen and pistil beyond the corolla). Light quality significantly influenced the absolute size of several floral traits as well as the allometry (i.e., relative scaling) of all floral traits, and genotypes differed in the plasticity of floral traits to the light treatments. Exposure to low relative to high R:FR resulted in significantly greater elongation in the vegetative trait, petiole length, and genotypes again differed in the plasticity of this trait to R:FR. Consistent with prior studies, most floral traits were less plastic than the vegetative trait; herkogamy (i.e., stigma-anther separation) was the exception and expressed more variable trait values across environments than petiole length, apparently as a consequence of the independent responses of stamens and pistils. Flowers also showed strong phenotypic integration; genotypic correlations were significantly positive among floral traits within each light treatment. Although floral-vegetative correlations were not significant in the high R:FR light treatment, significant correlations were detected between petal traits, pistil length, and petiole length under low R:FR, in contrast to the widely held hypothesis that floral and vegetative traits are genetically independent. Finally, we detected selection for reduced herkogamy in the low R:FR light treatment. The observed correlation between functional trait groups suggest that vegetative plasticity may affect the expression of floral traits in some environments, and that environment-specific constraints may exist on the evolution of floral and vegetative traits.     

THE GENOMIC ARCHITECTURE OF SEXUAL DIMORPHISM IN THE DIOECIOUS PLANT SILENE LATIFOLIA

Evaluating the genetic architecture of sexual dimorphism can aid our understanding of the extent to which shared genetic control of trait variation versus sex‐specific control impacts the evolutionary dynamics of phenotypic change within each sex. We performed a QTL analysis on Silene latifolia to evaluate the contribution of sex‐specific QTL to phenotypic variation in 46 traits, whether traits involved in trade‐offs had colocalized QTL, and whether the distribution of sex‐specific loci can explain differences between the sexes in their variance/covariance matrices. We used a backcross generation derived from two artificial‐selection lines. We found that sex‐specific QTL explained a significantly greater percent of the variation in sexually dimorphic traits than loci expressed in both sexes. Genetically correlated traits often had colocalized QTL, whose signs were in the expected direction. Lastly, traits with different genetic correlations within the sexes displayed a disproportionately high number of sex‐specific QTL, and more QTL co‐occurred in males than females, suggesting greater trait integration. These results show that sex differences in QTL patterns are congruent with theory on the resolution of sexual conflict and differences based on G ‐matrix results. They also suggest that trade‐offs and trait integration are likely to affect males more than females.     

Geographical differentiation in floral traits across the distribution range of the Patagonian oil-secreting Calceolaria polyrhiza: do pollinators matter?

Background and Aims

The underlying evolutionary processes of pollinator-driven floral diversification are still poorly understood. According to the Grant–Stebbins model speciation begins with adaptive local differentiation in the response to spatial heterogeneity in pollinators. Although this crucial process links the micro- and macroevolution of floral adaptation, it has received little attention. In this study geographical phenotypic variation was investigated in Patagonian Calceolaria polyrhiza and its pollinators, two oil-collecting bee species that differ in body size and geographical distribution.

Methods

Patterns of phenotypic variation were examined together with their relationships with pollinators and abiotic factors. Six floral and seven vegetative traits were measured in 45 populations distributed across the entire species range. Climatic and edaphic parameters were determined for 25 selected sites, 2–16 bees per site of the most frequent pollinator species were captured, and a critical flower–bee mechanical fitting trait involved in effective pollination was measured. Geographical patterns of phenotypic and environmental variation were examined using uni- and multivariate analyses. Decoupled geographical variation between corolla area and floral traits related to the mechanical fit of pollinators was explored using a Mantel test.

Key Results

The body length of pollinators and the floral traits related to mechanical fit were strongly correlated with each other. Geographical variation of the mechanical-fit-related traits was decoupled from variation in corolla size; the latter had a geographical pattern consistent with that of the vegetative traits and was mainly affected by climatic gradients.

Conclusions

The results are consistent with pollinators playing a key role in shaping floral phenotype at a geographical scale and promoting the differentiation of two floral ecotypes. The relationship between the critical floral-fit-related trait and bee length remained significant even in models that included various environmental variables and an allometric predictor (corolla area). The abiotic environment also has an important role, mainly affecting floral size. Decoupled geographical variation between floral mechanical-fit-related traits and floral size would represent a strategy to maintain plant–pollinator phenotypic matching in this environmentally heterogeneous area.     

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.     

Constraint and opportunity: the genetic basis and evolution of modularity in the cichlid mandible

Modular variation, whereby the relative degree of connectivity varies within a system, is thought to evolve through a process of selection that favors the integration of certain traits and the decoupling of others. In this way, modularity may facilitate the pace of evolution and determine evolvability. Alternatively, conserved patterns of modularity may act to constrain the rate and direction of evolution by preventing certain functions from evolving. A comprehensive understanding of the potential interplay between these phenomena will require knowledge of the inheritance and the genetic basis of modularity. Here we explore these ideas in the cichlid mandible by investigating patterns of modularity at the clade and species levels and through the introduction of a new approach, the individual level. Specifically, we assessed patterns of covariation in Lake Malawi cichlid species that employ alternate "biting" and "suction-feeding" modes of feeding and in a hybrid cross between these two ecotypes. Across the suction-feeding clade, patterns of modularity were largely conserved and reflected a functionally based pattern. In contrast, the biting species displayed a pattern of modularity that more closely matched developmental modules. The pattern of modularity present in our F2 population was very similar to the pattern exhibited by the biter, suggesting a role for dominant inheritance. We demonstrate that our individual-level metric of modularity (IMM) is a valid quantitative trait that has a nonlinear relationship with shape. IMMs for each model were used as quantitative characters to map quantitative trait loci (QTL) that underlie modularity. Our QTL analysis offers new insights into the genetic basis of modularity in these fishes that may eventually lead to the discovery of the genetic processes that delineate particular modules. In all, our findings suggest that modularity is both a constraining and an evolvable force in cichlid evolution, as distinct patterns occur between species and variation exists among individuals.     

Covariance of floral and vegetative traits in four species of Ranunculaceae: a comparison between specialized and generalized pollination systems

Theory predicts that tighter correlation between floral traits and weaker relationship between floral and vegetative traits more likely occur in specialized flowers than generalized flowers,favoring by precise fit with pollinators.However,traits and trait correlations frequently vary under different environments.Through detecting spatiotemporal variation in phenotypic traits (floral organ size and vegetative size) and trait correlations in four Ranunculaceae species,we examined four predictions.Overall,our results supported these predictions to a certain degree.The mean coefficient of variation (CV) of floral traits in two specialized species (Delphinium kamaonense and Aconitum gymnandrum) was marginally significantly lower than that of another two generalized species (Trollius ranunculoides and Anemone obtusiloba).The two specialized species also showed marginally significantly smaller CV in floral traits than vegetative size across the two species.The absolute mean correlation between floral and vegetative traits,or that between floral traits in species with specialized flowers was not significantly lower,or higher than that in generalized plants,weakly supporting the predictions.Furthermore,we documented a large variation in trait correlations of four species among different seasons and populations.Study of covariance of floral and vegetative traits will benefit from the contrast of results obtained from generalized and specialized pollination systems.     

Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon

Distinct floral pollination syndromes have emerged multiple times during the diversification of flowering plants. For example, in western North America, a hummingbird pollination syndrome has evolved more than 100 times, generally from within insect-pollinated lineages. The hummingbird syndrome is characterized by a suite of floral traits that attracts and facilitates pollen movement by hummingbirds, while at the same time discourages bee visitation. These floral traits generally include large nectar volume, red flower colour, elongated and narrow corolla tubes and reproductive organs that are exerted from the corolla. A handful of studies have examined the genetic architecture of hummingbird pollination syndrome evolution. These studies find that mutations of relatively large effect often explain increased nectar volume and transition to red flower colour. In addition, they suggest that adaptive suites of floral traits may often exhibit a high degree of genetic linkage, which could facilitate their fixation during pollination syndrome evolution. Here, we explore these emerging generalities by investigating the genetic basis of floral pollination syndrome divergence between two related Penstemon species with different pollination syndromes—bee-pollinated P. neomexicanus and closely related hummingbird-pollinated P. barbatus. In an F₂ mapping population derived from a cross between these two species, we characterized the effect size of genetic loci underlying floral trait divergence associated with the transition to bird pollination, as well as correlation structure of floral trait variation. We find the effect sizes of quantitative trait loci for adaptive floral traits are in line with patterns observed in previous studies, and find strong evidence that suites of floral traits are genetically linked. This linkage may be due to genetic proximity or pleiotropic effects of single causative loci. Interestingly, our data suggest that the evolution of floral traits critical for hummingbird pollination was not constrained by negative pleiotropy at loci that show co-localization for multiple traits.     

QTL analysis of floral traits in Louisiana iris hybrids

The formation of hybrid zones between nascent species is a widespread phenomenon. The evolutionary consequences of hybridization are influenced by numerous factors, including the action of natural selection on quantitative trait variation. Here we examine how the genetic basis of floral traits of two species of Louisiana Irises affects the extent of quantitative trait variation in their hybrids. Quantitative trait locus (QTL) mapping was used to assess the size (magnitude) of phenotypic effects of individual QTL, the degree to which QTL for different floral traits are colocalized, and the occurrence of mixed QTL effects. These aspects of quantitative genetic variation would be expected to influence (1) the number of genetic steps (in terms of QTL substitutions) separating the parental species phenotypes; (2) trait correlations; and (3) the potential for transgressive segregation in hybrid populations. Results indicate that some Louisiana Iris floral trait QTL have large effects and QTL for different traits tend to colocalize. Transgressive variation was observed for six of nine traits, despite the fact that mixed QTL effects influence few traits. Overall, our QTL results imply that the genetic basis of floral morphology and color traits might facilitate the maintenance of phenotypic divergence between Iris fulva and Iris brevicaulis, although a great deal of phenotypic variation was observed among hybrids.     

Covariance and decoupling of floral and vegetative traits in nine Neotropical plants: a re-evaluation of Berg's correlation-pleiades concept

Nearly forty years ago R. L. Berg proposed that plants with specialized pollination ecology evolve genetic and developmental systems that decouple floral morphology from phenotypic variation in vegetative traits. These species evolve separate floral and vegetative trait clusters, or as she termed them, "correlation pleiades." The predictions of this hypothesis have been generally supported, but only a small sample of temperate-zone herb and grass species has been tested. To further evaluate this hypothesis, especially its applicability to plants of other growth forms, we examined the patterns of phenotypic variation and covariation of floral and vegetative traits in nine species of Neotropical plants. We recognized seven specific predictions of Berg's hypothesis. Our results supported some predictions but not others. Species with specialized pollination systems usually had floral traits decoupled (weak correlation; Canna and Eichornia) or buffered (relationship with shallow proportional slope; Calathea and Canna) from variation in vegetative traits. However, the same trend was also observed in three species with unspecialized pollination systems (Echinodorus, Muntingia, and Wedelia). One species with unspecialized pollination (Croton) and one wind-pollinated species (Cyperus) showed no decoupling or buffering, as predicted. While species with specialized pollination usually showed lower coefficients of variation for floral traits than vegetative traits (as predicted), the same was also true of species with unspecialized or wind pollination (unlike our prediction). Species with specialized pollination showed less variation in floral traits than did species with unspecialized or wind pollination, as predicted. However, the same was true of the corresponding vegetative traits, which was unexpected. Also in contrast to our prediction, plants with specialized pollination systems did not exhibit tighter phenotypic integration of floral characters than did species with generalized pollination systems. We conclude that the patterns of morphological integration among floral traits and between floral and vegetative traits tend to be species specific, not easily predicted from pollination ecology, and generally more complicated than R. L. Berg envisaged.     

Functional decoupling between flowers and leaves in the Ameroglossum pernambucense complex can facilitate local adaptation across a pollinator and climatic heterogeneous landscape

Decoupling between floral and leaf traits is expected in plants with specialized pollination systems to assure a precise flower–pollinator fit, irrespective of leaf variation associated with environmental heterogeneity (functional modularity). Nonetheless, developmental interactions among floral traits also decouple flowers from leaves regardless of selection pressures (developmental modularity). We tested functional modularity in the hummingbird‐pollinated flowers of the Ameroglossum pernambucense complex while controlling for developmental modularity. Using two functional traits responsible for flower–pollinator fit [floral tube length (TL) and anther–nectary distance (AN)], one floral trait not linked to pollination [sepal length (SL), control for developmental modularity] and one leaf trait [leaf length (LL)], we found evidence of flower functional modularity. Covariation between TL and AN was ca. two‐fold higher than the covariation of either of these traits with sepal and leaf lengths, and variations in TL and AN, important for a precise flower–pollinator fit, were smaller than SL and LL variations. Furthermore, we show that previously reported among‐population variation of flowers associated with local pollinator phenotypes was independent from SL and LL variations. These results suggest that TL and AN are functionally linked to fit pollinators and sufficiently decoupled from developmentally related floral traits (SL) and vegetative traits (LL). These results support previous evidences of population differentiation due to local adaptation in the A. pernambucense complex and shed light on the role of flower–leaf decoupling for local adaptation in species distributed across biotic and abiotic heterogeneous landscapes.     

Quantitative trait loci for inflorescence development in Arabidopsis thaliana

Variation in inflorescence development patterns is a central factor in the evolutionary ecology of plants. The genetic architectures of 13 traits associated with inflorescence developmental timing, architecture, rosette morphology, and fitness were investigated in Arabidopsis thaliana, a model plant system. There is substantial naturally occurring genetic variation for inflorescence development traits, with broad sense heritabilities computed from 21 Arabidopsis ecotypes ranging from 0.134 to 0.772. Genetic correlations are significant for most (64/78) pairs of traits, suggesting either pleiotropy or tight linkage among loci. Quantitative trait locus (QTL) mapping indicates 47 and 63 QTL for inflorescence developmental traits in Ler x Col and Cvi x Ler recombinant inbred mapping populations, respectively. Several QTL associated with different developmental traits map to the same Arabidopsis chromosomal regions, in agreement with the strong genetic correlations observed. Epistasis among QTL was observed only in the Cvi x Ler population, and only between regions on chromosomes 1 and 5. Examination of the completed Arabidopsis genome sequence in three QTL regions revealed between 375 and 783 genes per region. Previously identified flowering time, inflorescence architecture, floral meristem identity, and hormone signaling genes represent some of the many candidate genes in these regions.     

Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible

The mouse mandible has long served as a model system for complex morphological structures. Here we use new methodology based on geometric morphometrics to test the hypothesis that the mandible consists of two main modules, the alveolar region and the ascending ramus, and that this modularity is reflected in the effects of quantitative trait loci (QTL). The shape of each mandible was analyzed by the positions of 16 morphological landmarks and these data were analyzed using Procrustes analysis. Interval mapping in the F(2) generation from intercrosses of the LG/J and SM/J strains revealed 33 QTL affecting mandible shape. The QTL effects corresponded to a variety of shape changes, but ordination or a parametric bootstrap test of clustering did not reveal any distinct groups of QTL that would affect primarily one module or the other. The correlations of landmark positions between the two modules tended to be lower than the correlations between arbitrary subsets of landmarks, indicating that the modules were relatively independent of each other and confirming the hypothesized location of the boundary between them. While these results are in agreement with the hypothesis of modularity, they also underscore that modularity is a question of the relative degrees to which QTL contribute to different traits, rather than a question of discrete sets of QTL contributing to discrete sets of traits.     

Modular genetic architecture of floral morphology in Nicotiana: quantitative genetic and comparative phenotypic approaches to floral integration

Animal‐pollinated flowers are complex structures that may require a precise configuration of floral organs for proper function. As such, they represent an excellent system with which we can examine the role of phenotypic integration and modularity in morphological evolution. We use complementary quantitative genetic and comparative phenotypic approaches to examine correlations among floral characters in Nicotiana alata, N. forgetiana and their artificial fourth‐generation hybrids. Flowers of both species share basic patterns of genetic and phenotypic correlations characterized by at least two integrated character suites that are relatively independent of each other and are not disrupted by four generations of recombination in hybrids. We conclude that these integrated character suites represent phenotypic modules that are the product of a modular genetic architecture. Intrafloral modularity may have been critical for rapid specialization of these species to different pollinators.     

Indirect effects of FRIGIDA: floral trait (co)variances are altered by seasonally variable abiotic factors associated with flowering time

Reproductive timing is a critical life‐history event that could influence the (co)variation of traits developing later in ontogeny by regulating exposure to seasonally variable factors. In a field experiment with Arabidopsis thaliana, we explore whether allelic variation at a flowering‐time gene of major effect (FRIGIDA) affects (co)variation of floral traits by regulating exposure to photoperiod, temperature, and moisture levels. We detect a positive latitudinal cline in floral organ size among plants with putatively functional FRI alleles. Statistically controlling for bolting day removes the cline, suggesting that seasonal abiotic variation affects floral morphology. Both photoperiod and precipitation at bolting correlate positively with the length of petals, stamens, and pistils. Additionally, floral (co)variances differ significantly across FRI backgrounds, such that the sign of some floral‐trait correlations reverses. Subsequent experimental manipulations of photoperiod and water availability demonstrate direct effects of these abiotic factors on floral traits. In sum, these results highlight how the timing of life‐history events can affect the expression of traits developing later in ontogeny, and provide some of the first empirical evidence for the effects of major genes on evolutionary potential.