A multivariate view of the evolution of sexual dimorphism.

Sexual differences are often dramatic and widespread across taxa. Their extravagance and ubiquity can be puzzling because the common underlying genome of males and females is expected to impede rather than foster phenotypic divergence. Widespread dimorphism, despite a shared genome, may be more readily explained by considering the multivariate, rather than univariate, framework governing the evolution of sexual dimorphism. In the univariate formulation, differences in genetic variances and a low intersexual genetic correlation (rMF) can facilitate the evolution of sexual dimorphism. However, studies that have analysed sex-specific differences in heritabilities or genetic variances do not always find significant differences. Furthermore, many of the reported estimates of rMF are very high and positive. When monomorphic heritabilities and a high rMF are present together, the evolution of sexual dimorphism on a trait-by-trait basis is severely constrained. By contrast, the multivariate formulation has greater generality and more flexibility. Although the number of multivariate sexual dimorphism studies is low, almost all support sex-specific differences in the G (variance-covariance) matrix; G matrices can differ with respect to size and/or orientation, affecting the response to selection differently between the sexes. Second, whereas positive values of the univariate quantity rMF only hinder positive changes in sexual dimorphism, positive covariances in the intersexual covariance B matrix can either help or hinder. Similarly, the handful of studies reporting B matrices indicate that it is often asymmetric, so that B can affect the evolution of single traits differently between the sexes. Multivariate approaches typically demonstrate that genetic covariances among traits can strongly constrain trait evolution when compared with univariate approaches. By contrast, in the evolution of sexual dimorphism, a multivariate view potentially reveals more opportunities for sexual dimorphism to evolve by considering the effect sex-specific selection has on sex-specific G matrices and an asymmetric B matrix.

Morning glory as a powerful model in ecological genomics: tracing adaptation through both natural and artificial selection.

Many diverse questions in ecology and evolution have been addressed using species belonging to the genus Ipomoea, commonly referred to as the morning glory genus. Ipomoea exhibits a wide range of diversity in floral color, growth form, mating system and tolerance to environmental factors, both within and among species, and as such has been a focal group of many investigations in the last 80 years. In this review, we highlight recent work to which Ipomoea species have contributed-from studies of the mating system, molecular evolution, plant-herbivore and plant-parasite interactions to their impact on and importance to agriculture. Genomic resources for this group are currently under development, and given the breadth of studies and history of this group, combined with an expanding genetics toolkit, we argue that Ipomoea should provide the next model organism for ecological genomics.

Mutualism variation in the nodulation response to nitrate.

The evolution of mutualisms under novel selective pressures will play a key role in ecosystem responses to environmental change. Because fixed nitrogen is traded in plant­rhizobium mutualisms, increasing N availability in the soil is predicted to alter coevolution of these interactions. Legumes typically decrease the number of associations (nodules) with rhizobia in response to nitrate, but the evolutionary dynamics of this response remain unknown. We grew plant and rhizobium genotype combinations in three N environments to assess the coevolutionary potential of the nodule nitrate response in natural communities of plants and rhizobia. We found evidence for coevolutionary genetic variation for nodulation in response to nitrate (G × G × E interaction), suggesting that the mutualism response to N deposition will depend on the combination of partner genotypes. Thus, the nitrate response is not a fixed mechanism in plant­rhizobium symbioses, but instead is potentially subject to natural selection and dynamic coevolution.

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.

Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits.

A central challenge in evolutionary biology is to identify genes underlying ecologically important traits and describe the fitness consequences of naturally occurring variation at these loci. To address this goal, several novel approaches have been developed, including 'population genomics,' where a large number of molecular markers are scored in individuals from different environments with the goal of identifying markers showing unusual patterns of variation, potentially due to selection at linked sites. Such approaches are appealing because of (1) the increasing ease of generating large numbers of genetic markers, (2) the ability to scan the genome without measuring phenotypes and (3) the simplicity of sampling individuals without knowledge of their breeding history. Although such approaches are inherently applicable to non-model systems, to date these studies have been limited in their ability to uncover functionally relevant genes. By contrast, quantitative genetics has a rich history, and more recently, quantitative trait locus (QTL) mapping has had some success in identifying genes underlying ecologically relevant variation even in novel systems. QTL mapping, however, requires (1) genetic markers that specifically differentiate parental forms, (2) a focus on a particular measurable phenotype and (3) controlled breeding and maintenance of large numbers of progeny. Here we present current advances and suggest future directions that take advantage of population genomics and quantitative genetic approaches - in both model and non-model systems. Specifically, we discuss advantages and limitations of each method and argue that a combination of the two provides a powerful approach to uncovering the molecular mechanisms responsible for adaptation.

Costs and benefits of cold tolerance in transgenic Arabidopsis thaliana.

Cold tolerance in plants is an ecologically important trait that has been under intensive study for basic and applied reasons. Determining the fitness benefits and costs of cold tolerance has previously been difficult because cold tolerance is normally an induced trait that is not expressed in warm environments. The recent creation of transgenic plants constitutively expressing cold tolerance genes enables the investigation of the fitness consequences of cold tolerance in multiple temperature environments. We studied three genes from the CBF (C-repeat/dehydration responsive element binding factor) cold tolerance pathway, CBF1, 2 and 3, in Arabidopsis thaliana to test for benefits and costs of constitutive cold tolerance. We used multiple insertion lines for each transgene and grew the lines in cold and control conditions. Costs of cold tolerance, as determined by fruit number, varied by individual transgene. CBF2 and 3 overexpressers showed costs of cold tolerance, and no fitness benefits, in both environments. CBF1 overexpressing plants showed no fitness cost of cold tolerance in the control environment and showed a marginal fitness benefit in the cold environment. These results suggest that constitutive expression of traits that are normally induced in response to environmental stress will not always lead to costs in the absence of that stress, and that the ecological risks of CBF transgene escape should be assessed prior to their use in commercial agriculture.

Flowering time plasticity in Arabidopsis thaliana: a reanalysis of Westerman & Lawrence (1970).

Environmental variation in temperature can have dramatic effects on plant morphology, phenology, and fitness, and for this reason it is important to understand the evolutionary dynamics of phenotypic plasticity in response to temperature. We investigated constraints on the evolution of phenotypic plasticity in response to a temperature gradient in the model plant Arabidopsis thaliana by applying modern analytical tools to the classic data of Westerman & Lawrence (1970). We found significant evidence for two types of constraints. First, we detected numerous significant genetic correlations between plastic responses to temperature and the mean value of a trait across all environments, which differed qualitatively in pattern between the set of ecotypes and the set of mutant lines in the original sample. Secondly, we detected significant costs of flowering time plasticity in two of the three experimental environments, and a net pattern of selection against flowering time plasticity in the experiment overall. Thus, when explored with contemporary methods, the prescient work of Westerman & Lawrence (1970) provides new insights about evolutionary constraints on the evolution of plasticity.

Diffuse selection on resistance to deer herbivory in the ivyleaf morning glory, Ipomoea hederacea.

Recent work defines coevolution between plants and herbivores as pairwise when the pattern of selection on resistance traits and the response to selection are both independent of the presence or absence of other herbivores. In addition, for a pairwise response to selection, resistance to a focal herbivore must have the same genetic basis in the presence and absence of other herbivores. None of these conditions were satisfied for the ivyleaf morning glory, Ipomoea hederacea, and its insect, fungal, and mammalian natural enemies with a quantitative genetics field experiment. A significant negative genetic correlation exists between resistance to deer and generalist insect herbivory that would preclude an independent response to selection. In addition, resistance loci under selection differ depending on the composition of the natural enemy community as indicated by genetic correlations between deer resistances in the presence and absence of other natural enemies that differ substantially from 1. Finally, selection on deer resistance depends on the presence or absence of insects; in the presence of insects, greater deer resistance is favored, but in the absence of insects, deer resistance is effectively neutral. These results indicate that the composition of the natural enemy community can alter both the pattern of selection and the likely response to selection of resistance traits.