The spatial scale of adaptation in a native annual plant and its implications for responses to climate change.

Spatial patterns of adaptation provide important insights into agents of selection and expected responses of populations to climate change. Robust inference into the spatial scale of adaptation can be gained through reciprocal transplant experiments that combine multiple source populations and common gardens. Here, we examine the spatial scale of local adaptation of the North American annual plant common ragweed, Ambrosia artemisiifolia, using data from four common gardens with 22 source populations sampled from across a ∼1200 km latitudinal gradient within the native range. We found evidence of local adaptation at the northernmost common garden, but maladaptation at the two southern gardens, where more southern source populations outperformed local populations. Overall, the spatial scale of adaptation was large-at the three gardens where distance between source populations and gardens explained variation in fitness, it took an average of 820 km for fitness to decline to 50% of its predicted maximum. Taken together, these results suggest that climate change has already caused maladaptation, especially across the southern portion of the range, and may result in northward range contraction over time.

Pleiotropy facilitates local adaptation to distant optima in common ragweed (Ambrosia artemisiifolia).

Pleiotropy, the control of multiple phenotypes by a single locus, is expected to slow the rate of adaptation by increasing the chance that beneficial alleles also have deleterious effects. However, a prediction arising from classical theory of quantitative trait evolution states that pleiotropic alleles may have a selective advantage when phenotypes are distant from their selective optima. We examine the role of pleiotropy in regulating adaptive differentiation among populations of common ragweed (Ambrosia artemisiifolia); a species that has recently expanded its North American range due to human-mediated habitat change. We employ a phenotype-free approach by using connectivity in gene networks as a proxy for pleiotropy. First, we identify loci bearing footprints of local adaptation, and then use genotype-expression mapping and co-expression networks to infer the connectivity of the genes. Our results indicate that the putatively adaptive loci are highly pleiotropic, as they are more likely than expected to affect the expression of other genes, and they reside in central positions within the gene networks. We propose that the conditionally advantageous alleles at these loci avoid the cost of pleiotropy by having large phenotypic effects that are beneficial when populations are far from their selective optima. We further use evolutionary simulations to show that these patterns are in agreement with a model where populations face novel selective pressures, as expected during a range expansion. Overall, our results suggest that highly connected genes may be targets of positive selection during environmental change, even though they likely experience strong purifying selection in stable selective environments.

Context Dependence of Local Adaptation to Abiotic and Biotic Environments: A Quantitative and Qualitative Synthesis.

Understanding how spatially variable selection shapes adaptation is an area of long-standing interest in evolutionary ecology. Recent meta-analyses have quantified the extent of local adaptation, but the relative importance of abiotic and biotic factors in driving population divergence remains poorly understood. To address this gap, we combined a quantitative meta-analysis and a qualitative metasynthesis to (1) quantify the magnitude of local adaptation to abiotic and biotic factors and (2) characterize major themes that influence the motivation and design of experiments that seek to test for local adaptation. Using local-foreign contrasts as a metric of local adaptation (or maladaptation), we found that local adaptation was greater in the presence than in the absence of a biotic interactor, especially for plants. We also found that biotic environments had stronger effects on fitness than abiotic environments when ignoring whether those environments were local versus foreign. Finally, biotic effects were stronger at low latitudes, and abiotic effects were stronger at high latitudes. Our qualitative analysis revealed that the lens through which local adaptation has been examined differs for abiotic and biotic factors. It also revealed biases in the design and implementation of experiments that make quantitative results challenging to interpret and provided directions for future research.

Does adaptation to historical climate shape plant responses to future rainfall patterns? A rainfall manipulation experiment with common ragweed.

Climate change is affecting both the volume and distribution of precipitation, which in turn is expected to affect the growth and reproduction of plant populations. The near ubiquity of local adaptation suggests that adaptive differentiation may have important consequences for how populations are affected by and respond to changing precipitation. Here, we manipulated rainfall in a common garden to examine how differentiation among populations of common ragweed, Ambrosia artemisiifolia (Asteraceae) affects responses to water availability expected under climate change. We collected seeds from 26 populations along gradients of historical rainfall and used event-based rainout shelters and watering additions to simulate drier summer conditions and more extreme rainfall events, respectively. Ambrosia artemisiifolia had higher fitness on average under reduced rainfall, suggesting it may spread and become more abundant in areas projected to become hotter and drier during the summer months. We also found strong evidence for phenotypic and fitness clines across both latitude and longitude, and that phenological responses and fitness effects of altered rainfall depended on seed source or historical climate. The effect of rainfall treatment on female fitness was highest in western and mid longitudes, but there was little effect on eastern populations. Across latitude, the effect of rainfall treatment on male fitness was highest in southern populations. These phenology and fitness clines suggest that adaptive differentiation across the species' range has the potential to shape future responses of A. artemisiifolia populations to climate change, particularly altered patterns of rainfall.

A roadmap for urban evolutionary ecology.

Urban ecosystems are rapidly expanding throughout the world, but how urban growth affects the evolutionary ecology of species living in urban areas remains largely unknown. Urban ecology has advanced our understanding of how the development of cities and towns change environmental conditions and alter ecological processes and patterns. However, despite decades of research in urban ecology, the extent to which urbanization influences evolutionary and eco-evolutionary change has received little attention. The nascent field of urban evolutionary ecology seeks to understand how urbanization affects the evolution of populations, and how those evolutionary changes in turn influence the ecological dynamics of populations, communities, and ecosystems. Following a brief history of this emerging field, this Perspective article provides a research agenda and roadmap for future research aimed at advancing our understanding of the interplay between ecology and evolution of urban-dwelling organisms. We identify six key questions that, if addressed, would significantly increase our understanding of how urbanization influences evolutionary processes. These questions consider how urbanization affects nonadaptive evolution, natural selection, and convergent evolution, in addition to the role of urban environmental heterogeneity on species evolution, and the roles of phenotypic plasticity versus adaptation on species' abundance in cities. Our final question examines the impact of urbanization on evolutionary diversification. For each of these six questions, we suggest avenues for future research that will help advance the field of urban evolutionary ecology. Lastly, we highlight the importance of integrating urban evolutionary ecology into urban planning, conservation practice, pest management, and public engagement.

Little plant, big city: a test of adaptation to urban environments in common ragweed (Ambrosia artemisiifolia).

A full understanding of how cities shape adaptation requires characterizing genetically-based phenotypic and fitness differences between urban and rural populations under field conditions. We used a reciprocal transplant experiment with the native plant common ragweed, (Ambrosia artemisiifolia), and found that urban and rural populations have diverged in flowering time, a trait that strongly affects fitness. Although urban populations flowered earlier than rural populations, plants growing in urban field sites flowered later than plants in rural field sites. This counter-gradient variation is consistent adaptive divergence between urban and rural populations. Also consistent with local adaptation, both urban and rural genotypes experienced stronger net selection in the foreign than in the local habitat, but this pattern was not significant for male fitness. Despite the evidence for local adaptation, rural populations had higher lifetime fitness at all sites, suggesting that selection has been stronger or more uniform in rural than urban populations. We also found that inter-population differences in both flowering time and fitness tended to be greater among urban than rural populations, which is consistent with greater drift or spatial variation in selection within urban environments. In summary, our results are consistent with adaptive divergence of urban and rural populations, but also suggest there may be greater environmental heterogeneity in urban environments which also affects evolution in urban landscapes.

The effect of leaf shape on the thermoregulation and frost tolerance of an annual vine, Ipomoea hederacea (Convolvulaceae).

PREMISE OF STUDY: Leaf shape is predicted to have important ecophysiological consequences; for example, theory predicts that lobed leaves should track air temperature more closely than their entire-margined counterparts. Hence, leaf-lobing may be advantageous during cold nights (∼0°C) when there is the risk of damage by radiation frost (a phenomenon whereby leaves fall below air temperature because of an imbalance between radiational heat loss and convective heat gain). METHODS: Here, we test whether radiation frost can lead to differential damage between leaf shapes by examining a leaf-shape polymorphism in Ipomoea hederacea, where leaves are either lobed or heart-shaped depending on a single Mendelian locus. We logged leaf temperature during midautumn, and measured chlorophyll fluorescence and survival as proxies of performance. Furthermore, we tested if the leaf-shape locus confers freezing tolerance using freezing assays on leaf tissue from different leaf shapes. KEY RESULTS: We found that lobed leaves consistently remain warmer than heart-shaped leaves during the night, but that no pattern emerged during the day, and that temperature differences between leaf shapes were typically small. Furthermore, we found that leaf types did not differ in frost tolerance, but that a 1°C decrease leads to a transition from moderate to complete damage. CONCLUSIONS: Our results demonstrate that Ipomoea hederacea leaf shapes do experience different nighttime temperatures, and that only minor temperature differences can lead to disparate levels of freezing damage, suggesting that the differential thermoregulation could result in different levels of frost damage.

Mapping the genetic basis of symbiotic variation in legume-rhizobium interactions in Medicago truncatula.

Mutualisms are known to be genetically variable, where the genotypes differ in the fitness benefits they gain from the interaction. To date, little is known about the loci that underlie such genetic variation in fitness or whether the loci influencing fitness are partner specific, and depend on the genotype of the interaction partner. In the legume-rhizobium mutualism, one set of potential candidate genes that may influence the fitness benefits of the symbiosis are the plant genes involved in the initiation of the signaling pathway between the two partners. Here we performed quantitative trait loci (QTL) mapping in Medicago truncatula in two different rhizobium strain treatments to locate regions of the genome influencing plant traits, assess whether such regions are dependent on the genotype of the rhizobial mutualist (QTL × rhizobium strain), and evaluate the contribution of sequence variation at known symbiosis signaling genes. Two of the symbiotic signaling genes, NFP and DMI3, colocalized with two QTL affecting average fruit weight and leaf number, suggesting that natural variation in nodulation genes may potentially influence plant fitness. In both rhizobium strain treatments, there were QTL that influenced multiple traits, indicative of either tight linkage between loci or pleiotropy, including one QTL with opposing effects on growth and reproduction. There was no evidence for QTL × rhizobium strain or genotype × genotype interactions, suggesting either that such interactions are due to small-effect loci or that more genotype-genotype combinations need to be tested in future mapping studies.