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Habitat restoration may depend on the recovery of plant microbial symbionts such as arbuscular mycorrhizal (AM) fungi, but this requires a better understanding of the rules that govern their community assembly. We examined the interactions of soil and host-associated AM fungal communities between remnant and restored patches of subtropical montane forests. While AM fungal richness did not differ between habitat types, community membership did and was influenced by geography, habitat and host. These differences were largely driven by rare host-specific AM fungi that displayed near-complete turnover between forest types, while core AM fungal taxa were highly abundant and ubiquitous. The bipartite networks in the remnant forest were more specialized and hosts more specific than in the restored forest. Host-associated AM fungal communities nested within soil communities in both habitats, but only significantly so in the restored forest. Our results provide evidence that restored and remnant forests harbour the same core fungal symbionts, while rare host-specific taxa differ, and that geography, host identity and taxonomic resolution strongly affect the observed distribution patterns of these fungi. We suggest that host-specific interactions with AM fungi, as well as spatial processes, should be explicitly considered to effectively re-establish target host and symbiont communities.

Premise Across taxa, vegetative and floral traits that vary along a fast-slow life-history axis are often correlated with leaf functional traits arrayed along the leaf economics spectrum, suggesting a constrained set of adaptive trait combinations. Such broad-scale convergence may arise from genetic constraints imposed by pleiotropy (or tight linkage) within species, or from natural selection alone. Understanding the genetic basis of trait syndromes and their components is key to distinguishing these alternatives and predicting evolution in novel environments. Methods We used a line-cross approach and quantitative trait locus (QTL) mapping to characterize the genetic basis of twenty leaf functional/physiological, life history, and floral traits in hybrids between annualized and perennial populations of scarlet monkeyflower (Mimulus cardinalis). Results We mapped both single and multi-trait QTLs for life history, leaf function and reproductive traits, but found no evidence of genetic co-ordination across categories. A major QTL for three leaf functional traits (thickness, photosynthetic rate, and stomatal resistance) suggests that a simple shift in leaf anatomy may be key to adaptation to seasonally dry habitats. Conclusions Our results suggest that the co-ordination of resource-acquisitive leaf physiological traits with a fast life-history and more selfing mating system results from environmental selection rather than functional or genetic constraint. Independent assortment of distinct trait modules, as well as a simple genetic basis to leaf physiological traits associated with drought escape, may facilitate adaptation to changing climates.

Many traits covary with environmental gradients to form phenotypic clines. While local adaptation to the environment can generate phenotypic clines, other nonadaptive processes may also. If local adaptation causes phenotypic clines, then the direction of genotypic selection on traits should shift from one end of the cline to the other. Traditionally, genotypic selection on non-Gaussian traits like germination rate have been hampered because it is challenging to measure their genetic variance.Here we used quantitative genetics and reciprocal transplants to test whether a previously discovered cline in germination rate showed additional signatures of adaptation in the scarlet monkeyflower (Mimulus cardinalis). We measured genotypic and population level covariation between germination rate and early survival, a component of fitness. We developed a novel discrete log-normal model to estimate genetic variance in germination rate.Contrary to our adaptive hypothesis, we found no evidence that genetic variation in germination rate contributed to variation in early survival. Across populations, southern populations in both gardens germinated earlier and survived more.Southern populations have higher early survival but it is not caused by faster germination. This pattern is consistent with nonadaptive forces driving the phenotypic cline in germination rate, but future work will need to assess whether there is selection at other life stages. This statistical framework should help expand quantitative genetic analyses for other waiting-time traits.

International audience; Leaf optical properties impact leaf energy balance and thus leaf temperature. The effect of leaf development on mid-infrared (MIR) reflectance, and hence thermal emissivity, has not been investigated in detail. We measured a suite of morphological characteristics, as well as directional-hemispherical reflectance from ultraviolet to thermal infrared wavelengths (250 nm to 20 µm) of leaves from five temperate deciduous tree species over the 8 wk following spring leaf emergence. By contrast to reflectance at shorter wavelengths, the shape and magnitude of MIR reflectance spectra changed markedly with development. MIR spectral differences among species became more pronounced and unique as leaves matured. Comparison of reflectance spectra of intact vs dried and ground leaves points to cuticular developmentand not internal structural or biochemical changesas the main driving factor. Accompanying the observed spectral changes was a drop in thermal emissivity from about 0.99 to 0.95 over the 8 wk following leaf emergence. Emissivity changes were not large enough to substantially influence leaf temperature, but they could potentially lead to a bias in radiometrically measured temperatures of up to 3 K. Our results also pointed to the potential for using MIR spectroscopy to better understand species-level differences in cuticular development and composition.

PremiseMany traits covary with environmental gradients to form phenotypic clines. While local adaptation to the environment can generate phenotypic clines, other nonadaptive processes may also. If local adaptation causes phenotypic clines, then the direction of genotypic selection on traits should shift from one end of the cline to the other. Traditionally genotypic selection on non-Gaussian traits like germination rate have been hampered because it is challenging to measure their genetic variance.MethodsHere we used quantitative genetics and reciprocal transplants to test whether a previously discovered cline in germination rate showed additional signatures of adaptation in the scarlet monkeyflower (Mimulus cardinalis). We measured genotypic and population level covariation between germination rate and early survival, a component of fitness. We developed a novel discrete log-normal model to estimate genetic variance in germination rate.ResultsContrary to our adaptive hypothesis, we found no evidence that genetic variation in germination rate contributed to variation in early survival. Across populations, southern populations in both gardens germinated earlier and survived more.ConclusionsSouthern populations have higher early survival but this is not caused by faster germination. This pattern is consistent with nonadaptive forces driving the phenotypic cline in germination rate, but future work will need to assess whether there is selection at other life stages. This statistical framework should help expand quantitative genetic analyses for other waiting-time traits.

Functional and developmental constraints on phenotypic variation may cause traits to covary over millions of years and slow populations from reaching their adaptive optima. Alternatively, trait covariation may result from selective constraint if some trait combinations are generally maladaptive. Quantifying the relative contribution of functional, developmental, and selective constraints on phenotypic variation is a longstanding goal of macroevolution, but it is often difficult to distinguish different types of constraints. The anatomy of leaves with stomata on both surfaces (amphistomatous) present a unique opportunity to test the importance of functional and developmental constraints on phenotypyic evolution. The key insight is that stomata on each leaf surface encounter the same functional and developmental constraints, but potentially different selective constraints because of leaf asymmetry in light capture, gas exchange, and other features. Independent evolution of stomatal traits on each surface imply that functional and developmental constraints alone likely do not explain trait covariance. Packing limits on how many stomata can fit into a finite epidermis and cell-size-mediated developmental integration are hypothesized to constrain variation in stomatal anatomy. The simple geometry of the planar leaf surface and knowledge of stomatal development make it possible to derive equations for phenotypic (co)variance caused by these constraints and compare them with data. We analyzed evolutionary covariance between stomatal density and length in amphistomatous leaves from 236 phylogenetically independent contrasts using a robust Bayesian model. Stomatal anatomy on each surface diverges partially independently, meaning that packing limits and developmental integration are not sufficient to explain phenotypic (co)variation. Hence, selective constraints, which require an adaptive explanation, likely contribute to (co)variation in ecologically important traits like stomata. We show how it is possible to evaluate the contribution of different constraints by deriving expected patterns of (co)variance and testing them using similar but separate tissues, organs, or sexes.

Plant ecophysiology is founded on a rich body of physical and chemical theory, but it is challenging to connect theory with data in unambiguous, analytically rigorous and reproducible ways. Custom scripts written in computer programming languages (coding) enable plant ecophysiologists to model plant processes and fit models to data reproducibly using advanced statistical techniques. Since many ecophysiologists lack formal programming education, we have yet to adopt a unified set of coding principles and standards that could make coding easier to learn, use and modify. We identify eight principles to help in plant ecophysiologists without much programming experience to write resilient code: (i) standardized nomenclature, (ii) consistency in style, (iii) increased modularity/extensibility for easier editing and understanding, (iv) code scalability for application to large data sets, (v) documented contingencies for code maintenance, (vi) documentation to facilitate user understanding; (vii) extensive tutorials and (viii) unit testing and benchmarking. We illustrate these principles using a new R package, {photosynthesis}, which provides a set of analytical and simulation tools for plant ecophysiology. Our goal with these principles is to advance scientific discovery in plant ecophysiology by making it easier to use code for simulation and data analysis, reproduce results and rapidly incorporate new biological understanding and analytical tools., Tired: Remembering whether ‘ACi_solanum_C_final.xlsx’ or ‘ACi_solanum_D_v3.xlsx’ has the correct parameter estimates. Wired: Using reproducible, scalable, open-source code to analyse your ecophysiological data. Get started with a gentle introduction to eight principles of coding and an R software package called photosynthesis! We cover naming functions and variables, style, modularity, scalability, documenting contingencies, help documentation, tutorials and testing. The photosynthesis package implements these principles for gas exchange and hydraulic curve fitting and modelling.

While the fundamental biophysics of C 3 photosynthesis is highly conserved across plants, substantial leaf structural and enzymatic variation translates into variability in rates of carbon assimilation. Although this variation is well documented, it remains poorly understood how photosynthetic rates evolve, and whether macroevolutionary changes are related to the evolution of leaf morphology and biochemistry. A substantial challenge in large-scale comparative studies is disentangling evolutionary adaptation from environmental acclimation. We overcome this by using a ‘macroevolutionary common garden’ approach in which we measured metabolic traits ( J max and V cmax ) from 111 phylogenetically diverse species in a shared environment. We find substantial phylogenetic signal in these traits at moderate phylogenetic timescales, but this signal dissipates quickly at deeper scales. Morphological traits exhibit phylogenetic signal over much deeper timescales, suggesting that these are less evolutionarily constrained than metabolic traits. Furthermore, while morphological and biochemical traits (LMA, N area and C area ) are weakly predictive of J max and V c max , evolutionary changes in these traits are mostly decoupled from changes in metabolic traits. This lack of tight evolutionary coupling implies that it may be incorrect to use changes in these functional traits in response to global change to infer that photosynthetic strategy is also evolving.

The size and density of stomatal pores limit the maximum rate of leaf carbon gain and water loss (gmax) in land plants. The limits of gmax due to anatomy, and its constraint by the negative correlation of stomatal size and density at broad phylogenetic scales, has been unclear and controversial. The prevailing hypothesis posits that adaptation to higher gmax is typically constrained by geometry and/or an economic need to reduce the allocation of epidermal area to stomata (stomatal-area minimization), and this would require the evolution of greater numbers of smaller stomata. Another view, supported by the data, is that across plant diversity, epidermal area allocated to guard cells versus other cells can be optimized without major trade-offs, and higher gmax would typically be achieved with a higher allocation of epidermal area to stomata (stomatal-area increase). We tested these hypotheses by comparing their predictions for the structure of the covariance of stomatal size and density across species, applying macroevolutionary models and phylogenetic regression to data for 2408 species of angiosperms, gymnosperms, and ferns from forests worldwide. The observed stomatal size-density scaling and covariance supported the stomatal-area increase hypothesis for high gmax. A higher gmax involves construction costs and maintenance costs that should be considered in models assessing optimal stomatal conductance for predictions of water use, photosynthesis, and water-use efficiency as influences on crop productivity or in Earth System models.

Anthropogenic climate change is generating mismatches between the environmental conditions that populations historically experienced and those in which they reside. Understanding how climate change affects population performance is a critical scientific challenge. We combine a quantitative synthesis of field transplant experiments with a novel statistical approach based in evolutionary theory to quantify the effects of temperature and precipitation variability on population performance. We find that species’ average performance is affected by both temperature and precipitation, but populations show signs of local adaptation to temperature only. Contemporary responses to temperature are strongly shaped by the local climates under which populations evolved, resulting in performance declines when temperatures deviate from historic conditions. Adaptation to other local environmental factors is strong, but temperature deviations as small as 2°C erode the advantage that these non-climatic adaptations historically gave populations in their home sites.One sentence summaryClimate change is pulling the thermal rug out from under populations, reducing average performance and eroding their historical home-site advantage.

PREMISEAcross taxa, vegetative and floral traits that vary along a fast-slow life-history axis are often correlated with leaf functional traits arrayed along the leaf economics spectrum, suggesting a constrained set of adaptive trait combinations. Such broad-scale convergence may arise from genetic constraints imposed by pleiotropy (or tight linkage) within species, or from natural selection alone. Understanding the genetic basis of trait syndromes and their components is key to distinguishing these alternatives and predicting evolution in novel environments.METHODSWe used a line-cross approach and quantitative trait locus (QTL) mapping to characterize the genetic basis of twenty leaf functional/physiological, life history, and floral traits in hybrids between annualized and perennial populations of scarlet monkeyflower (Mimulus cardinalis).RESULTSWe mapped both single and multi-trait QTLs for life history, leaf function and reproductive traits, but found no evidence of genetic co-ordination across categories. A major QTL for three leaf functional traits (thickness, photosynthetic rate, and stomatal resistance) suggests that a simple shift in leaf anatomy may be key to adaptation to seasonally dry habitats.CONCLUSIONSOur results suggest that the co-ordination of resource-acquisitive leaf physiological traits with a fast life history and more selfing mating system results from environmental selection rather than functional or genetic constraint. Independent assortment of distinct trait modules, as well as a simple genetic basis to leaf physiological traits associated with drought escape, may facilitate adaptation to changing climates.

The acquisitive-conservative axis of plant ecological strategies results in a pattern of leaf trait covariation that captures the balance between leaf construction costs and plant growth potential. Studies evaluating trait covariation within species are scarcer, and have mostly dealt with variation in response to environmental gradients. Little work has been published on intraspecific patterns of leaf trait covariation in the absence of strong environmental variation.Methods: We analysed covariation of four leaf functional traits (SLA: specific leaf area, LDMC: leaf dry matter content, Ft: force to tear, and Nm: leaf nitrogen content) in six Poaceae and four Fabaceae species common in the dry Chaco forest of Central Argentina, growing in the field and in a common garden. We compared intraspecific covariation patterns (slopes, correlation and effect size) of leaf functional traits with global interspecific covariation patterns. Additionally, we checked for possible climatic and edaphic factors that could affect the intraspecific covariation pattern.Key Results: We found negative correlations for the LDMC-SLA, Ft-SLA, LDMC-Nm , and Ft-Nm trait pairs. This intraspecific covariation pattern found both in the field and in the common garden and not be explained by climatic or edaphic variation in the field follows the expected acquisitive-conservative axis. At the same time, we found quantitative differences in slopes among different species, and between these intraspecific patterns and the interspecific ones. Many of these differences seem to be idiosyncratic, but some appear consistent among species (e.g.all the intraspecific LDMC-SLA and LDMC-Nm slopes tend to be shallower than the global).Conclusions: Our study indicates that the acquisitive-conservative leaf functional trait covariation pattern occurs at the intraspecific level even in the absence of relevant environmental variation in the field. This suggests a high degree of variation-covariation in leaf functional traits not driven by environmental variables. Fil: Gorne, Lucas Damián. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas, Físicas y Naturales; Argentina Fil: Díaz, Sandra Myrna. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas, Físicas y Naturales; Argentina Fil: Minden, Vanessa. University of Oldenburg; Alemania. Vrije Universiteit Brussel; Bélgica Fil: Onoda, Yusuke. Kyoto University. School of Agriculture; Japón Fil: Kramer, Koen. Wageningen University; Países Bajos Fil: Muir, Christopher. University Of Hawaii; Estados Unidos Fil: Michaletz, Sean T. University of British Columbia; Canadá Fil: Lavorel, Sandra. Centre National de la Recherche Scientifique; Francia Fil: Sharpe, Joanne. Sharplex Services, Edgecomb; Estados Unidos Fil: Jansen, Steven. Universitat Ulm; Alemania Fil: Slot, Martijn. Smithsonian Tropical Research Institute; Panamá Fil: Chacon, Maximiliano Eduardo. Universidad de Costa Rica; Costa Rica Fil: Boenisch, Gerhard. Max Planck Institute For Biogeochemistry; Alemania

Stomatal pores control both leaf gas exchange and are one route for infection of internal plant tissues by many foliar pathogens, setting up the potential for tradeoffs between photosynthesis and defense. Anatomical shifts to lower stomatal density and/or size may also limit pathogen colonization, but such developmental changes could permanently reduce the gas exchange capacity for the life of the leaf. I developed and analyzed a spatially explicit model of pathogen colonization on the leaf as a function of stomatal size and density, anatomical traits which partially determine maximum rates of gas exchange. The model predicts greater stomatal size or density increases the probability of colonization, but the effect is most pronounced when the fraction of leaf surface covered by stomata is low. I also derived scaling relationships between stomatal size and density that preserves a given probability of colonization. These scaling relationships set up a potential anatomical conflict between limiting pathogen colonization and minimizing the fraction of leaf surface covered by stomata. Although a connection between gas exchange and pathogen defense has been suggested empirically, this is the first mathematical model connecting gas exchange and pathogen defense via stomatal anatomy. A limitation of the model is that it does not include variation in innate immunity and stomatal closure in response to pathogens. Nevertheless, the model makes predictions that can be tested with experiments and may explain variation in stomatal anatomy among plants. The model is generalizable to many types of pathogens, but lacks significant biological realism that may be needed for precise predictions.

Trait integration arises through both selection on functional coordination and shared developmental pathways. Different anatomical components must both work well and develop together to generate individuals with the appropriate physiology to survive and reproduce in their environment. In this study, we used a common garden experiment and Bayesian multilevel models to test whether stomatal anatomy coordinates leaf gas exchange, Rubisco kinetics, and leaf size across 10 closely related species of Limonium from the Balearic Islands. The results indicate that the anatomical determinants of maximum stomatal conductance, stomatal density and size, were functionally coordinated with Rubisco kinetics – species whose stomatal anatomy was correlated with low stomatal conductance have evolved Rubisco enzymes better adapted to low operational chloroplastic CO2 concentrations. Lower stomatal density was associated with greater leaf size, which can be explained by a greater proportion of pavement cells in large-leaved species. These results suggest that both selection for functional coordination (stomata and Rubisco kinetics) and shared development pathways (stomatal density and leaf area) likely shape patterns of trait integration between species.

The genus Mimulus is a well-studied group of plant species, which has for decades allowed researchers to address a wide array of fundamental questions in biology (Wu & al. 2008; Twyford & al. 2015). Linnaeus named the type species of Mimulus (ringens L.), while Darwin (1876) used Mimulus (luteus L.) to answer key research questions. The incredible phenotypic diversity of this group has made it the focus of ecological and evolutionary study since the mid-20th century, initiated by the influential work of Clausen, Keck, and Hiesey as well as their students and collaborators (Clausen & Hiesey 1958; Hiesey & al. 1971, Vickery 1952, 1978). Research has continued on this group of diverse taxa throughout the 20th and into the 21st century (Bradshaw & al. 1995; Schemske & Bradshaw 1999; Wu & al. 2008; Twyford & al. 2015; Yuan 2019), and Mimulus guttatus was one of the first non-model plants to be selected for full genome sequencing (Hellsten & al. 2013). Mimulus has played a key role in advancing our general understanding of the evolution of pollinator shifts (Bradshaw & Schemske 2003; Cooley & al. 2011; Byers & al. 2014), adaptation (Lowry & Willis 2010; Kooyers & al. 2015; Peterson & al. 2016; Ferris & Willis 2018; Troth & al. 2018), speciation (Ramsey & al. 2003; Wright & al. 2013; Sobel & Streisfeld 2015; Zuellig & Sweigart 2018), meiotic drive (Fishman & Saunders 2008), polyploidy (Vallejo-Marín 2012; Vallejo-Marín & al. 2015), range limits (Angert 2009; Sexton et al. 2011; Grossenbacher & al. 2014; Sheth & Angert 2014), circadian rhythms (Greenham & al. 2017), genetic recombination (Hellsten & al. 2013), mating systems (Fenster & Ritland 1994; Dudash & Carr 1998; Brandvain & al. 2014) and developmental biology (Moody & al. 1999; Baker & al. 2011, 2012; Yuan 2019). This combination of a rich history of study coupled with sustained modern research activity is unparalleled among angiosperms. Across many interested parties, the name Mimulus therefore takes on tremendous biological significance and is recognizable not only by botanists, but also by zoologists, horticulturalists, naturalists, and members of the biomedical community. Names associated with a taxonomic group of this prominence should have substantial inertia, and disruptive name changes should be avoided. As members of the Mimulus community, we advocate retaining the genus name Mimulus to describe all monkeyflowers. This is despite recent nomenclature changes that have led to a renaming of most monkeyflower species to other genera.

Beneficial microbes such as plant mutualistic fungi, hold the promise of ameliorating challenges faced in native plant conservation such as disease management. As an alternative to costly chemical pest control, conservation efforts could potentially harness the benefits of plant mutualistic fungi to aid in defense and disease resistance, but there are few tests of this notion. We set out to test the efficacy of controlling a common foliar pathogen, the powdery mildew Neoerysiphe galeopsidis, by inoculating the endangered Hawaiian plant species Phyllostegia kaalaensis with potentially beneficial members of its wild-type mycobiome. We tested whether inoculating plants with above or belowground fungal mutualists, or both, led to increased disease resistance in the host. We found that while all treatments reduced average disease incidence, colonization by the foliar yeast Moesziomyces aphidis was the only treatment to do so significantly. These results provide an exciting new strategy for plant conservation practices.

Plants must regulate leaf temperature to optimize photosynthesis, control water loss and prevent damage caused by overheating or freezing. Physical models of leaf energy budgets calculate the energy fluxes and leaf temperatures for a given set leaf and environmental parameters. These models can provide deep insight into the variation in leaf form and function, but there are few computational tools available to use these models. Here I introduce a new R package called tealeaves to make complex leaf energy budget models accessible to a broader array of plant scientists. This package enables novice users to start modelling leaf energy budgets quickly while allowing experts to customize their parameter settings. The code is open source, freely available and readily integrates with other R tools for scientific computing. This paper describes the current functionality of tealeaves, but new features will be added in future releases. This software tool will advance new research on leaf thermal physiology to advance our understanding of basic and applied plant science., tealeaves is a new R package to implement complex, customizable leaf energy budget models as part of an open source, transparent workflow.

Climate can affect plant populations through direct effects on physiology and fitness, and through indirect effects on their relationships with pollinating mutualists. We therefore expect that geographic variation in climate might lead to variation in plant mating systems. Biogeographic processes, such as range expansion, can also contribute to geographic patterns in mating system traits. We manipulated pollinator access to plants in eight sites spanning the geographic range of Clarkia pulchella to investigate geographic and climatic drivers of fruit production and seed set in the absence of pollinators (reproductive assurance). We examined how reproductive assurance and fruit production varied with the position of sites within the range of the species and with temperature and precipitation. We found that reproductive assurance in C. pulchella was greatest in populations in the northern part of the species’ range and was not well explained by any of the climate variables that we considered. In the absence of pollinators, some populations of C. pulchella have the capacity to increase fruit production, perhaps through resource reallocation, but this response is climate dependent. Pollinators are important for reproduction in this species, and recruitment is sensitive to seed input. The degree of autonomous self-pollination that is possible in populations of this mixed-mating species may be shaped by historic biogeographic processes or variation in plant and pollinator community composition rather than variation in climate.

The West-Brown-Enquist (WBE) metabolic scaling theory posits that many organismal features scale predictably with body size because of selection to minimize transport costs in resource distribution networks. Many scaling exponents are quarter-powers, as predicted by WBE, but there are also biologically significant deviations that could reflect adaptation to different environments. A central but untested prediction of the WBE model is that wide deviation from optimal scaling is penalized, leading to a pattern of constraint on scaling exponents. Here, we demonstrate, using phylogenetic comparative methods, that variation in allometric scaling between mass and leaf area across 17 wild tomato taxa is constrained around a value indistinguishable from that predicted by WBE but significantly greater than 2/3 (geometric-similarity model). The allometric-scaling exponent was highly correlated with fecundity, water use, and drought response, suggesting that it is functionally significant and therefore could be under selective constraints. However, scaling was not strictly log-log linear but rather declined during ontogeny in all species, as has been observed in many plant species. We caution that although our results supported one prediction of the WBE model, it did not strongly test the model in other important respects. Nevertheless, phylogenetic comparative methods such as those used here are powerful but underutilized tools for metabolic ecology that complement existing methods to adjudicate between models.

Hybrid incompatibilities contribute to reproductive isolation between species, allowing them to follow independent evolutionary trajectories. Since hybrid incompatibilities are by definition deleterious, they cannot be selected for directly and must arise as a by-product of evolutionary divergence. Divergent resolution of duplicate genes, a special case of Dobzhansky-Muller incompatibilities, is one mechanism by which hybrid incompatibility can evolve. Following whole-genome duplication, loss of gene copies could possibly increase the opportunity for divergent resolution and, hence, the evolution of hybrid incompatibilities. However, divergent resolution can take place only when populations are isolated in allopatry; genes lost within a species cannot contribute to future speciation. Furthermore, nearly complete allopatry is necessary for passive divergent resolution. Using mathematical models, we demonstrate that these two factors severely impede the ability of divergent resolution alone to increase speciation rates, except under very particular conditions. Instead, we find that the population dynamics of diverging lineages dominate this process, leading to a larger role for ecology relative to genetics in the origin of new species, even by passive mechanisms. Divergent resolution of duplicate genes might increase speciation rates in some clades at some times, but our results indicate that it alone is unlikely to account for the macroevolutionary success of polyploid clades.

Local adaptation is commonly observed in nature: organisms perform well in their natal environment, but poorly outside it. Correlations between traits and latitude, or latitudinal clines, are among the most common pieces of evidence for local adaptation, but identifying the traits under selection and the selective agents is challenging. Here, we investigated a latitudinal cline in growth and photosynthesis across 16 populations of the perennial herbErythranthe cardinalis(Phrymaceae). Using machine learning methods, we identify interannual variation in precipitation as a likely selective agent: Southern populations from more variable environments had higher photosynthetic rates and grew faster. We hypothesize that selection may favor a more annualized life history – grow now rather than save for next year – in environments where severe droughts occur more often. Thus our study provides insight into how species may adapt if Mediterranean climates become more variable due to climate change.

Natural selection on photosynthetic performance is a primary factor determining leaf phenotypes. The complex CO2 diffusion path from substomatal cavities to the chloroplasts – the mesophyll conductance (gm) – limits photosynthetic rate in many species and hence shapes variation in leaf morphology and anatomy. Among sclerophyllous and succulent taxa, structural investment in leaves, measured as the leaf dry mass per area (LMA), has been implicated in decreased gm. However, in herbaceous taxa with high gm, it is less certain how LMA impacts CO2 diffusion and whether it significantly affects photosynthetic performance. We addressed these questions in the context of understanding the ecophysiological significance of leaf trait variation in wild tomatoes, a closely related group of herbaceous perennials. Although gm was high in wild tomatoes, variation in gm significantly affected photosynthesis. Even in these tender-leaved herbaceous species, greater LMA led to reduced gm. This relationship between gm and LMA is partially mediated by cell packing and leaf thickness, although amphistomy (equal distribution of stomata on both sides of the leaf) mitigates the effect of leaf thickness. Understanding the costs of increased LMA will inform future work on the adaptive significance of leaf trait variation across ecological gradients in wild tomatoes and other systems.

Adult leaf fenestration in "Swiss cheese" plants (Monstera Adans.) is an unusual leaf shape trait lacking a convincing evolutionary explanation. Monstera are secondary hemiepiphytes that inhabit the understory of tropical rainforests, where photosynthesis from sunflecks often makes up a large proportion of daily carbon assimilation. Here I present a simple model of leaf-level photosynthesis and whole-plant canopy dynamics in a stochastic light environment. The model demonstrates that leaf fenestration can reduce the variance in plant growth and thereby increase geometric mean fitness. This growth-variance hypothesis also suggests explanations for conspicuous ontogenetic changes in leaf morphology (heteroblasty) in Monstera, as well as the absence of leaf fenestration in co-occurring juvenile tree species. The model provides a testable hypothesis of the adaptive significance of a unique leaf shape and illustrates how variance in growth rate could be an important factor shaping plant morphology and physiology.

Species barriers, expressed as hybrid inviability and sterility, are often due to epistatic interactions between divergent loci from two lineages. Theoretical models indicate that the strength, direction, and complexity of these genetic interactions can strongly affect the expression of interspecific reproductive isolation and the rates at which new species evolve. Nonetheless, empirical analyses have not quantified the frequency with which loci are involved in interactions affecting hybrid fitness, and whether these loci predominantly interact synergistically or antagonistically, or preferentially involve loci that have strong individual effects on hybrid fitness. We systematically examined the prevalence of interactions between pairs of short chromosomal regions from one species (Solanum habrochaites) co-introgressed into a heterospecific genetic background (Solanum lycopersicum), using lines containing pairwise combinations of 15 chromosomal segments from S. habrochaites in the background of S. lycopersicum (i.e., 95 double introgression lines). We compared the strength of hybrid incompatibility (either pollen sterility or seed sterility) expressed in each double introgression line to the expected additive effect of its two component single introgressions. We found that epistasis was common among co-introgressed regions. Interactions for hybrid dysfunction were substantially more prevalent in pollen fertility compared to seed fertility phenotypes, and were overwhelmingly antagonistic (i.e., double hybrids were less unfit than expected from additive single introgression effects). This pervasive antagonism is expected to attenuate the rate at which hybrid infertility accumulates among lineages over time (i.e., giving diminishing returns as more reproductive isolation loci accumulate), as well as decouple patterns of accumulation of sterility loci and hybrid incompatibility phenotypes. This decoupling effect might explain observed differences between pollen and seed fertility in their fit to theoretical predictions of the accumulation of isolation loci, including the ‘snowball’ effect., Author summary A characteristic feature of new species is their inability to produce fertile or viable hybrids with other lineages. This post-zygotic reproductive isolation is caused by dysfunctional interactions between genes that have newly evolved changes in the diverging lineages. Whether these interactions occur between pairs of divergent alleles, or involve more complex networks of genes, can have strong effects on how rapidly reproductive isolation—and therefore new species—evolve. The complexity of these interactions, however, is poorly understood in empirical systems. We examined the fertility of hybrids that carried one or two chromosomal regions from a close relative, finding that hybrids with two of these heterospecific regions were frequently less sterile than would be expected from the joint fitness of hybrids that have the same regions singly. This ‘less-than-additive’ effect on hybrid sterility was widespread (observed in 20% of pairwise combinations), and especially pronounced for male sterility. We infer that genes contributing to male sterility form a more tightly connected network than previously thought, implying that reproductive isolation is evolving by incremental dysfunction of complex interactions rather than by independent pairwise incompatibilities. We use simulations to illustrate these expected patterns of accumulation of reproductive isolation when it involves highly interconnected gene networks.

Although traditionally separated by different aims and methodologies, research on agricultural and evolutionary problems shares a common goal of understanding the mechanisms underlying functionally important traits. As such, research in both fields offers potential complementary and reciprocal insights. Here, we discuss adaptive stress responses (specifically to water stress) as an example of potentially fruitful research reciprocity, where agricultural research has clearly produced advances that could benefit evolutionary studies, while evolutionary studies offer approaches and insights underexplored in crop studies. We focus on research on Solanum species that include the domesticated tomato and its wild relatives. Integrated approaches to understanding ecological adaptation are particularly attractive in tomato and its wild relatives: many presumptively adaptive phenotypic differences characterize wild species, and the physiological and mechanistic basis of many relevant traits and environmental responses has already been examined in the context of cultivated tomato and some wild species. We highlight four specific instances where these reciprocal insights can be combined to better address questions that are fundamental both to agriculture and evolution.

Are organisms free to reach their adaptive optima or constrained by hard-wired developmental programs? Recent evidence suggests that the arrangement of stomata on abaxial (lower) and adaxial (upper) leaf surfaces may be an important adaptation in plants, but stomatal traits on each surface likely share developmental pathways that could hamper evolution. We reviewed the quantitative genetics of stomatal density to look for loci that (1) affected ab- or adaxial density independently or (2) pleiotropically affected stomatal density on both surfaces. We also used phylogenetic comparative methods to test for independent versus correlated evolution of stomatal traits (density, size, and pore index) on each surface from 14 amphistomatous wild tomato taxa (Solanum; Solanaceae). Naturally occurring and laboratory-induced genetic variation alters stomatal density on one surface without affecting the other, indicating that development does not strongly constrain the spectrum of available mutations. Among wild tomato taxa, traits most closely related to function (stomatal pore index and density) evolved independently on each surface, whereas stomatal size was constrained by correlated evolution. Genetics and phylogenetics demonstrate mostly independent evolution of stomatal function on each leaf surface, facilitating largely unfettered access to fitness optima.

Natural selection may often favor coordination between different traits, or phenotypic integration, in order to most efficiently acquire and deploy scarce resources. As leaves are the primary photosynthetic organ in plants, many have proposed that leaf physiology, biochemistry, and anatomical structure are coordinated along a functional trait spectrum from fast, resource-acquisitive syndromes to slow, resource-conservative syndromes. However, the coordination hypothesis has rarely been tested at a phylogenetic scale most relevant for understanding rapid adaptation in the recent past or predicting evolutionary trajectories in response to climate change. To that end, we used a common garden to examine genetically-based coordination between leaf traits across 19 wild and cultivated tomato taxa. We found surprisingly weak integration between photosynthetic rate, leaf structure, biochemical capacity, and CO2 diffusion, even though all were arrayed in the predicted direction along a 'fast-slow' spectrum. This suggests considerable scope for unique trait combinations to evolve in response to new environments or in crop breeding. In particular, we find that partially independent variation in stomatal and mesophyll conductance may allow a plant to improve water-use efficiency without necessarily sacrificing maximum photosynthetic rates. Our study does not imply that functional trait spectra or tradeoffs are unimportant, but that the many important axes of variation within a taxonomic group may be unique and not generalizable to other taxa.

Ecologically important traits do not evolve without limits. Instead, evolution is constrained by the set of available and viable phenotypes. In particular, natural selection may only favour a narrow range of adaptive optima constrained within selective regimes. Here, I integrate data with theory to test whether selection explains phenotypic constraint. A global database of 599 plant species from 94 families shows that stomatal ratio, a trait affecting photosynthesis and defence against pathogens, is highly constrained. Most plants have their stomata on the lower leaf surface (hypostomy), but species with half their stomata on each surface (amphistomy) form a distinct mode in the trait distribution. A model based on a trade-off between maximizing photosynthesis and a fitness cost of upper stomata predicts a limited number of adaptive solutions, leading to a multimodal trait distribution. Phylogenetic comparisons show that amphistomy is the most common among fast-growing species, supporting the view that CO 2 diffusion is under strong selection. These results indicate that selective optima stay within a relatively stable set of selective regimes over macroevolutionary time.

Adaptive evolution requires both raw genetic material and an accessible path of high fitness from one fitness peak to another. In this study, we used an introgression line (IL) population to map quantitative trait loci (QTL) for leaf traits thought to be associated with adaptation to precipitation in wild tomatoes (Solanum sect. Lycopersicon; Solanaceae). A QTL sign test showed that several traits likely evolved under directional natural selection. Leaf traits correlated across species do not share a common genetic basis, consistent with a scenario in which selection maintains trait covariation unconstrained by pleiotropy or linkage disequilibrium. Two large effect QTL for stomatal distribution colocalized with key genes in the stomatal development pathway, suggesting promising candidates for the molecular bases of adaptation in these species. Furthermore, macroevolutionary transitions between vastly different stomatal distributions may not be constrained when such large-effect mutations are available. Finally, genetic correlations between stomatal traits measured in this study and data on carbon isotope discrimination from the same ILs support a functional hypothesis that the distribution of stomata affects the resistance to CO2 diffusion inside the leaf, a trait implicated in climatic adaptation in wild tomatoes. Along with evidence from previous comparative and experimental studies, this analysis indicates that leaf traits are an important component of climatic niche adaptation in wild tomatoes and demonstrates that some trait transitions between species could have involved few, large-effect genetic changes, allowing rapid responses to new environmental conditions.

Natural selection on photosynthetic performance is a primary factor determining leaf phenotypes. The complex CO2 diffusion path from substomatal cavities to the chloroplasts - the mesophyll conductance (g(m)) - limits photosynthetic rate in many species and hence shapes variation in leaf morphology and anatomy. Among sclerophyllous and succulent taxa, structural investment in leaves, measured as the leaf dry mass per area (LMA), has been implicated in decreased gm . However, in herbaceous taxa with high g(m), it is less certain how LMA impacts CO2 diffusion and whether it significantly affects photosynthetic performance. We addressed these questions in the context of understanding the ecophysiological significance of leaf trait variation in wild tomatoes, a closely related group of herbaceous perennials. Although g(m) was high in wild tomatoes, variation in g(m) significantly affected photosynthesis. Even in these tender-leaved herbaceous species, greater LMA led to reduced g(m). This relationship between g(m) and LMA is partially mediated by cell packing and leaf thickness, although amphistomy (equal distribution of stomata on both sides of the leaf) mitigates the effect of leaf thickness. Understanding the costs of increased LMA will inform future work on the adaptive significance of leaf trait variation across ecological gradients in wild tomatoes and other systems.

Genome-scale scans have revealed highly heterogeneous levels of divergence between closely related taxa in many systems. Generally, a small number of regions show high differentiation, with the rest of the genome showing no or only low levels of divergence. These patterns have been interpreted as evidence for ongoing speciation-with-gene-flow, with introgression homogenizing the whole genome except loci involved in reproductive isolation. However, as the number of selected loci increases, the probability of introgression at unselected loci decreases unless there is a transmission ratio distortion causing an over-representation of specific combinations of alleles. Here we examine the transmission of three ‘speciation islands’ that contain fixed differences between the M and S forms of the mosquito,Anopheles gambiae. We made reciprocal crosses between M and S parents and genotyped over 2000 F2individuals, developing a hierarchical likelihood model to identify specific genotypes that are under- or over-represented among the recombinant offspring. Though our overall results did not match the expected number of F2genotypes, we found no biased co-transmission among M or S alleles in the three islands. Our likelihood model did identify transmission ratio distortion at two of the three islands, but this distortion was small (approx. 3%) and in opposite directions for the two islands. We discuss how our results impinge on hypotheses of current gene flow between M and S and ongoing speciation-with-gene-flow in this system.

Like many species, the model plant Arabidopsis thaliana exhibits multiple different life histories in natural environments. We grew mutants impaired in different signaling pathways in field experiments across the species' native European range in order to dissect the mechanisms underlying this variation. Unexpectedly, mutational loss at loci implicated in the cold requirement for flowering had little effect on life history except in late-summer cohorts. A genetically informed photothermal model of progression toward flowering explained most of the observed variation and predicted an abrupt transition from autumn flowering to spring flowering in late-summer germinants. Environmental signals control the timing of this transition, creating a critical window of acute sensitivity to genetic and climatic change that may be common for seasonally regulated life history traits.