Effects of urban-induced mutations on ecology, evolution and health.

Increasing evidence suggests that urbanization is associated with higher mutation rates, which can affect the health and evolution of organisms that inhabit cities. Elevated pollution levels in urban areas can induce DNA damage, leading to de novo mutations. Studies on mutations induced by urban pollution are most prevalent in humans and microorganisms, whereas studies of non-human eukaryotes are rare, even though increased mutation rates have the potential to affect organisms and their populations in contemporary time. Our Perspective explores how higher mutation rates in urban environments could impact the fitness, ecology and evolution of populations. Most mutations will be neutral or deleterious, and higher mutation rates associated with elevated pollution in urban populations can increase the risk of cancer in humans and potentially other species. We highlight the potential for urban-driven increased deleterious mutational loads in some organisms, which could lead to a decline in population growth of a wide diversity of organisms. Although beneficial mutations are expected to be rare, we argue that higher mutation rates in urban areas could influence adaptive evolution, especially in organisms with short generation times. Finally, we explore avenues for future research to better understand the effects of urban-induced mutations on the fitness, ecology and evolution of city-dwelling organisms.

Phenotypic lags influence rapid evolution throughout a drought cycle.

Climate anomalies are increasing and posing strong selection, which can lead to rapid evolution. This is occurring on a backdrop of interannual variability that might weaken or even reverse selection. However, the effect of interannual climatic variability on rapid evolution is rarely considered. We study the climatic differences that contribute to rapid evolution throughout a seven-year period encompassing a severe drought across 12 populations of Mimulus cardinalis (scarlet monkeyflower). Plants were grown in a common greenhouse environment under wet and dry treatments, where specific leaf area and date of flowering were measured. We examine the association between trait values and different climate metrics at different time-periods, including the collection year, prior years, and cumulative metrics across sequential years. Of the climatic variables we assessed, we find that anomalies in mean annual precipitation best describe trait differences over our study period. Past climates, of one- to two years prior, are often related to trait values in a conflicting direction to collection-year climate. Uncovering these complex climatic impacts on evolution is critical to better predict and interpret the impacts of climate change.

Does urbanisation lead to parallel demographic shifts across the world in a cosmopolitan plant?

Urbanisation is occurring globally, leading to dramatic environmental changes that are altering the ecology and evolution of species. In particular, the expansion of human infrastructure and the loss and fragmentation of natural habitats in cities is predicted to increase genetic drift and reduce gene flow by reducing the size and connectivity of populations. Alternatively, the 'urban facilitation model' suggests that some species will have greater gene flow into and within cities leading to higher diversity and lower differentiation in urban populations. These alternative hypotheses have not been contrasted across multiple cities. Here, we used the genomic data from the GLobal Urban Evolution project (GLUE), to study the effects of urbanisation on non-adaptive evolutionary processes of white clover (Trifolium repens) at a global scale. We found that white clover populations presented high genetic diversity and no evidence of reduced Ne linked to urbanisation. On the contrary, we found that urban populations were less likely to experience a recent decrease in effective population size than rural ones. In addition, we found little genetic structure among populations both globally and between urban and rural populations, which showed extensive gene flow between habitats. Interestingly, white clover displayed overall higher gene flow within urban areas than within rural habitats. Our study provides the largest comprehensive test of the demographic effects of urbanisation. Our results contrast with the common perception that heavily altered and fragmented urban environments will reduce the effective population size and genetic diversity of populations and contribute to their isolation.

Global urban environmental change drives adaptation in white clover.

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

Regional differences in rapid evolution during severe drought.

Climate change is increasing drought intensity, threatening biodiversity. Rapid evolution of drought adaptations might be required for population persistence, particularly in rear-edge populations that may already be closer to physiological limits. Resurrection studies are a useful tool to assess adaptation to climate change, yet these studies rarely encompass the geographic range of a species. Here, we sampled 11 populations of scarlet monkeyflower (Mimulus cardinalis), collecting seeds across the plants' northern, central, and southern range to track trait evolution from the lowest to the greatest moisture anomaly over a 7-year period. We grew families generated from these populations across well-watered and terminal drought treatments in a greenhouse and quantified five traits associated with dehydration escape and avoidance. When considering pre-drought to peak-drought phenotypes, we find that later date of flowering evolved across the range of M. cardinalis, suggesting a shift away from dehydration escape. Instead, traits consistent with dehydration avoidance evolved, with smaller and/or thicker leaves evolving in central and southern regions. The southern region also saw a loss of plasticity in these leaf traits by the peak of the drought, whereas flowering time remained plastic across all regions. This observed shift in traits from escape to avoidance occurred only in certain regions, revealing the importance of geographic context when examining adaptations to climate change.

Adaptation across geographic ranges is consistent with strong selection in marginal climates and legacies of range expansion.

Every species experiences limits to its geographic distribution. Some evolutionary models predict that populations at range edges are less well adapted to their local environments due to drift, expansion load, or swamping gene flow from the range interior. Alternatively, populations near range edges might be uniquely adapted to marginal environments. In this study, we use a database of transplant studies that quantify performance at broad geographic scales to test how local adaptation, site quality, and population quality change from spatial and climatic range centers toward edges. We find that populations from poleward edges perform relatively poorly, both on average across all sites (15% lower population quality) and when compared to other populations at home (31% relative fitness disadvantage), consistent with these populations harboring high genetic load. Populations from equatorial edges also perform poorly on average (18% lower population quality) but, in contrast, outperform foreign populations (16% relative fitness advantage), suggesting that populations from equatorial edges have strongly adapted to unique environments. Finally, we find that populations from sites that are thermally extreme relative to the species' niche demonstrate strong local adaptation, regardless of their geographic position. Our findings indicate that both nonadaptive processes and adaptive evolution contribute to variation in adaptation across species' ranges.

Pelagic fish predation is stronger at temperate latitudes than near the equator.

Species interactions are widely thought to be strongest in the tropics, potentially contributing to the greater number of species at lower latitudes. Yet, empirical tests of this "biotic interactions" hypothesis remain limited and often provide mixed results. Here, we analyze 55 years of catch per unit effort data from pelagic longline fisheries to estimate the strength of predation exerted by large predatory fish in the world's oceans. We test two central tenets of the biotic interactions hypothesis: that predation is (1) strongest near the equator, and (2) positively correlated with species richness. Counter to these predictions, we find that predation is (1) strongest in or near the temperate zone and (2) negatively correlated with oceanic fish species richness. These patterns suggest that, at least for pelagic fish predation, common assumptions about the latitudinal distribution of species interactions do not apply, thereby challenging a leading explanation for the latitudinal gradient in species diversity.

Ellagitannins from the Onagraceae Decrease the Performance of Generalist and Specialist Herbivores.

Phenolics have a role in defenses against herbivores, but the defensive functions of specific groups of phenolics are still poorly understood. For example, ellagitannins (a type of hydrolyzable tannin) are predicted to decrease insect herbivore performance, but the effect of different types of ellagitannins on generalist and specialist herbivores has rarely been assessed. Here, we test the effects of the dominant oligomeric ellagitannins of Oenothera biennis and other Onagraceae on herbivore performance. We fed artificial diets containing between 1 and 100 mg/g of polyphenol fractions comprised of varying amounts and compositions of dimeric oenothein B, the trimeric oenothein A and larger oligomers, to one generalist (Spodoptera exigua) and one specialist (Schinia florida) insect herbivore species. We compared the effects of these ellagitannin fractions on herbivore performance to the effects of artificial diet containing total phenolic extracts from O. biennis, which contained these ellagitannins as well as many additional phenolic metabolites including flavonoid glycosides and caffeic acid derivatives. Both the ellagitannin fractions and O. biennis phenolic extracts had strong negative effects on S. exigua and S. florida performance, with stronger effects on the generalist herbivore. Differences between the effects of the various ellagitannin fractions were small and depended on insect life stage. The defensive effects of these ellagitannins were large, with lethal concentrations as low as 0.1% of the diet. These results highlight the important defensive function of ellagitannins against specialist and generalist herbivores and the need to characterize the effects of these understudied phenolics.

Testing for latitudinal gradients in defense at the macroevolutionary scale.

Plant defenses against herbivores are predicted to evolve to be greater in warmer climates, such as lower latitudes where herbivore pressure is also thought to be higher. Instead, recent findings are often inconsistent with this expectation, suggesting alternative hypotheses are needed. We tested for latitudinal gradients in plant defense evolution at the macroevolutionary scale by characterizing plant chemical defenses across 80 species of the evening primroses, spanning both North and South America. We quantified phenolics in leaves, flowers, and fruits, using advanced analytical chemistry techniques. Dominant individual ellagitannin compounds, total concentrations of ellagitannins, flavonoids, total phenolics, and compound diversity were quantified. Variation in these compounds was predicted with latitude, temperature, precipitation, and continent using phylogenetic generalized least squares (PGLS) multiple regression models. Latitude did not strongly explain variation in chemical defenses. Instead, fruit total ellagitannins, oenothein A, and total phenolics were greater in species inhabiting regions with colder climates. Using analytical chemistry and 80 species in two continents, we show that contrary to classic predictions, concentrations of secondary metabolites are not greater at lower latitudes or in warmer regions. We propose higher herbivore pressure in colder climates and gradients in resource availability as potential drivers of the observed patterns in Oenothera.

Latitudinal Gradients in Induced and Constitutive Resistance against Herbivores.

Plants are hypothesized to evolve increased defense against herbivores at lower latitudes, but an increasing number of studies report evidence that contradicts this hypothesis. Few studies have examined the evolution of constitutive and induced resistance along latitudinal gradients. When induction is not considered, underlying patterns of latitudinal clines in resistance can be obscured because plant resistance represents a combination of induced and constitutive resistance, which may show contrasting patterns with latitude. Here, we asked if there are latitudinal gradients in constitutive versus induced resistance by using genotypes of Oenothera biennis (Onagraceae) sampled along an 18° latitudinal gradient. We conducted two bioassay experiments to compare the resistance of plant genotypes against one generalist (Spodoptera exigua) and one specialist (Acanthoscelidius acephalus) herbivore. These insects were assayed on: i) undamaged control plants, ii) plants that had been induced with jasmonic acid, and iii) plants induced with herbivore damage. Additionally, we examined latitudinal gradients of constitutive and induced chemical resistance by measuring the concentrations of total phenolics, the concentration of oxidized phenolics, and the percentage of phenolics that were oxidized. Spodoptera exigua showed lower performance on plants from lower latitudes, whereas A. acephalus showed no latitudinal pattern. Constitutive total phenolics were greater in plants from lower latitudes, but induced plants showed higher total phenolics at higher latitudes. Oxidative activity was greatest at higher latitudes regardless of induction. Overall, both latitude and induction have an impact on different metrics of plant resistance to herbivory. Further studies should consider the effect of induction and herbivore specialization more explicitly, which may help to resolve the controversy in latitudinal gradients in herbivory and defense.

Sources of Controversy Surrounding Latitudinal Patterns in Herbivory and Defense.

Both herbivory and plant defenses against herbivores have been predicted to increase toward tropical regions. Early tests of this latitudinal herbivory-defense hypothesis (LHDH) were supportive, but accumulating evidence has been mixed. We argue that the lack of clarity might be due to heterogeneity in methodology and problems with study design and interpretation. We suggest possible solutions. Latitudinal studies need to carefully consider spatial and phylogenetic scale, to link plant defense measurements to herbivore performance, and to incorporate additional concepts from plant defense theory such as tolerance and induced defense. In addition, we call for consistent measures of herbivory to standardize comparisons across biomes. Improving methodology in future studies of LHDH should resolve much of the current controversy.

Can genetically based clines in plant defence explain greater herbivory at higher latitudes?

Greater plant defence is predicted to evolve at lower latitudes in response to increased herbivore pressure. However, recent studies question the generality of this pattern. In this study, we tested for genetically based latitudinal clines in resistance to herbivores and underlying defence traits of Oenothera biennis. We grew plants from 137 populations from across the entire native range of O. biennis. Populations from lower latitudes showed greater resistance to multiple specialist and generalist herbivores. These patterns were associated with an increase in total phenolics at lower latitudes. A significant proportion of the phenolics were driven by the concentrations of two major ellagitannins, which exhibited opposing latitudinal clines. Our analyses suggest that these findings are unlikely to be explained by local adaptation of herbivore populations or genetic variation in phenology. Rather greater herbivory at high latitudes can be explained by latitudinal clines in the evolution of plant defences.

Integrating landscape genomics and spatially explicit approaches to detect loci under selection in clinal populations.

Uncovering the genetic basis of adaptation hinges on the ability to detect loci under selection. However, population genomics outlier approaches to detect selected loci may be inappropriate for clinal populations or those with unclear population structure because they require that individuals be clustered into populations. An alternate approach, landscape genomics, uses individual-based approaches to detect loci under selection and reveal potential environmental drivers of selection. We tested four landscape genomics methods on a simulated clinal population to determine their effectiveness at identifying a locus under varying selection strengths along an environmental gradient. We found all methods produced very low type I error rates across all selection strengths, but elevated type II error rates under "weak" selection. We then applied these methods to an AFLP genome scan of an alpine plant, Campanula barbata, and identified five highly supported candidate loci associated with precipitation variables. These loci also showed spatial autocorrelation and cline patterns indicative of selection along a precipitation gradient. Our results suggest that landscape genomics in combination with other spatial analyses provides a powerful approach for identifying loci potentially under selection and explaining spatially complex interactions between species and their environment.

Dispersal analysis of three Peltigera species based on landscape genetics data.

Lichens can either disperse sexually through fungal spores or asexually through vegetative propagules and fragmentation. Understanding how genetic variation in lichens is distributed across a landscape can be useful to infer dispersal and establishment events in space and time as well as the conditions needed for this establishment. Most studies have sampled lichens across large spatial distances on the order of hundreds of kilometers, while here we sequence the internal transcribed spacer (ITS) for 113 samples of three Peltigera species sampling at a variety of small spatial scales. The maximum distance between sampled lichens was 3.7 km and minimum distance was approximately 20 cm. We find significant amounts of genetic diversity across all three species. For P. praetextata, two out of the three most common ITS genotypes exhibit spatial autocorrelation supporting short-range dispersal. Using rarefaction we estimate that all ITS genotypes in our sampling area have been found for P. praetextata and P. evansiana, but not P. canina. Comparing our results with other ITS data in the literature provides evidence for global dispersal for at least one sequence followed by the evolution of endemic haplotypes with wide dispersal and rare haplotypes with more local dispersal.