Local climate change velocities and evolutionary history explain multidirectional range shifts in a North American butterfly assemblage.

Species are often expected to shift their distributions either poleward or upslope to evade warming climates and colonise new suitable climatic niches. However, from 18-years of fixed transect monitoring data on 88 species of butterfly in the midwestern United States, we show that butterflies are shifting their centroids in all directions, except towards regions that are warming the fastest (southeast). Butterflies shifted their centroids at a mean rate of 4.87 km year-1. The rate of centroid shift was significantly associated with local climate change velocity (temperature by precipitation interaction), but not with mean climate change velocity throughout the species' ranges. Species tended to shift their centroids at a faster rate towards regions that are warming at slower velocities but increasing in precipitation velocity. Surprisingly, species' thermal niche breadth (range of climates butterflies experience throughout their distribution) and wingspan (often used as metric for dispersal capability) were not correlated with the rate at which species shifted their ranges. We observed high phylogenetic signal in the direction species shifted their centroids. However, we found no phylogenetic signal in the rate species shifted their centroids, suggesting less conserved processes determine the rate of range shift than the direction species shift their ranges. This research shows important signatures of multidirectional range shifts (latitudinal and longitudinal) and uniquely shows that local climate change velocities are more important in driving range shifts than the mean climate change velocity throughout a species' entire range.

Physiology evolves convergently but lags behind warming in cities.

Cities, through the generation of urban heat islands, provide a venue for exploring contemporary convergent evolution to climatic warming. We quantified how repeatable the evolution of heat tolerance, cold tolerance, and body size were among diverse lineages in response to urban heat islands. Our study revealed significant shifts towards higher heat tolerance and diminished cold tolerance among urban populations. We further found that the magnitude of trait divergence was significantly and positively associated with the magnitude of the urban heat island, suggesting that temperature played a major role in the observed divergence in thermal tolerance. Despite these trends, the magnitude of trait responses lagged behind environmental warming. Heat tolerance responses exhibited a deficit of 0.84°C for every 1°C increase in warming, suggesting limits on adaptive evolution and consequent adaptational lags. Other moderators were predictive of greater divergence in heat tolerance, including lower baseline tolerance and greater divergence in body size. Although terrestrial species did not exhibit systematic shifts towards larger or smaller body size, aquatic species exhibited significant shifts towards smaller body size in urban habitats. Our study demonstrates how cities can be used to address long-standing questions in evolutionary biology regarding the repeatability of evolution. Importantly, this work also shows how cities can be used as forecasting tools by quantifying adaptational lags and by developing trait-based associations with responses to contemporary warming.

Evidence of plasticity, but not evolutionary divergence, in the thermal limits of a highly successful urban butterfly.

Despite the generally negative impact of urbanization on insect biodiversity, some insect species persist in urban habitats. Understanding the mechanisms underpinning the ability of insects to tolerate urban habitats is critical given the contribution of land-use change to the global insect decline. Compensatory mechanisms such as phenotypic plasticity and evolutionary change in thermal physiological traits could allow urban populations to persist under the altered thermal regimes of urban habitats. It is important to understand the contributions of plasticity and evolution to trait change along urbanization gradients as the two mechanisms operate under different constraints and timescales. Here, we examine the plastic and evolutionary responses of heat and cold tolerance (critical thermal maximum [CTmax] and critical thermal minimum [CTmin]) to warming among populations of the cabbage white butterfly, Pieris rapae, from urban and non-urban (rural) habitats using a two-temperature common garden experiment. Although we expected populations experiencing urban warming to exhibit greater CTmax and diminished CTmin through plastic and evolutionary mechanisms, our study revealed evidence only for plasticity in the expected direction of both thermal tolerance traits. We found no evidence of evolutionary divergence in either heat or cold tolerance, despite each trait showing evolutionary potential. Our results suggest that thermal tolerance plasticity contributes to urban persistence in this system. However, as the magnitude of the plastic response was low and comparable to other insect species, other compensatory mechanisms likely further underpin this species' success in urban habitats.

Single-fly assemblies fill major phylogenomic gaps across the Drosophilidae Tree of Life.

Long-read sequencing is driving rapid progress in genome assembly across all major groups of life, including species of the family Drosophilidae, a longtime model system for genetics, genomics, and evolution. We previously developed a cost-effective hybrid Oxford Nanopore (ONT) long-read and Illumina short-read sequencing approach and used it to assemble 101 drosophilid genomes from laboratory cultures, greatly increasing the number of genome assemblies for this taxonomic group. The next major challenge is to address the laboratory culture bias in taxon sampling by sequencing genomes of species that cannot easily be reared in the lab. Here, we build upon our previous methods to perform amplification-free ONT sequencing of single wild flies obtained either directly from the field or from ethanol-preserved specimens in museum collections, greatly improving the representation of lesser studied drosophilid taxa in whole-genome data. Using Illumina Novaseq X Plus and ONT P2 sequencers with R10.4.1 chemistry, we set a new benchmark for inexpensive hybrid genome assembly at US $150 per genome while assembling genomes from as little as 35 ng of genomic DNA from a single fly. We present 183 new genome assemblies for 179 species as a resource for drosophilid systematics, phylogenetics, and comparative genomics. Of these genomes, 62 are from pooled lab strains and 121 from single adult flies. Despite the sample limitations of working with small insects, most single-fly diploid assemblies are comparable in contiguity (>1Mb contig N50), completeness (>98% complete dipteran BUSCOs), and accuracy (>QV40 genome-wide with ONT R10.4.1) to assemblies from inbred lines. We present a well-resolved multi-locus phylogeny for 360 drosophilid and 4 outgroup species encompassing all publicly available (as of August 2023) genomes for this group. Finally, we present a Progressive Cactus whole-genome, reference-free alignment built from a subset of 298 suitably high-quality drosophilid genomes. The new assemblies and alignment, along with updated laboratory protocols and computational pipelines, are released as an open resource and as a tool for studying evolution at the scale of an entire insect family.

Life cycle complexity and body mass drive erratic changes in climate vulnerability across ontogeny in a seasonally migrating butterfly.

Physiological traits are often used for vulnerability assessments of organismal responses to climate change. Trait values can change dramatically over the life cycle of organisms but are typically assessed at a single developmental stage. Reconciling ontogenetic changes in physiological traits with vulnerability assessments often reveals early life-stage vulnerabilities. The degree to which ontogenetic changes in physiological traits are due to changes in body mass over development versus stage-specific responses determines the degree to which mass can be used as a proxy for vulnerability. Here, we use the painted lady butterfly, Vanessa cardui, to test ontogenetic changes in two physiological traits, the acute thermal sensitivity of routine metabolic rate (RMR Q10) and the critical thermal maximum (CTmax). RMR Q10 generally followed ontogenetic changes in body mass, with stages characterized by smaller body mass exhibiting lower acute thermal sensitivity. However, CTmax was largely decoupled from ontogenetic changes in body mass. In contrast with trends from other studies showing increasing vulnerability among progressively earlier developmental stages, our study revealed highly erratic patterns of vulnerability across ontogeny. Specifically, we found the lowest joint-trait vulnerability (both RMR Q10 and CTmax) in the earliest developmental stage we tested (3rd instar larvae), the highest vulnerabilities in the next two developmental stages (4th and 5th instar larvae), and reduced vulnerability into the pupal and adult stages. Our study supports growing evidence of mechanistic decoupling of physiology across developmental stages and suggests that body mass is not a universal proxy for all physiological trait indicators of climate vulnerability.

Keep your cool: Overwintering physiology in response to urbanization in the acorn ant, Temnothorax curvispinosus.

Winter presents a challenge for survival, yet temperate ectotherms have remarkable physiological adaptations to cope with low-temperature conditions. Under recent climate change, rather than strictly relaxing pressure on overwintering survival, warmer winters can instead disrupt these low-temperature trait-environment associations, with negative consequences for populations. While there is increasing evidence of physiological adaptation to contemporary warming during the growing season, the effects of winter warming on physiological traits are less clear. To address this knowledge gap, we performed a common garden experiment using relatively warm-adapted versus cold-adapted populations of the acorn ant, Temnothorax curvispinosus, sampled across an urban heat island gradient, to explore the effects of winter conditions on plasticity and evolution of physiological traits. We found no evidence of evolutionary divergence in chill coma recovery nor in metabolic rate at either of two test temperatures (4 and 10 °C). Although we found the expected plastic response of increased metabolic rate under the 10 °C acute test temperature as compared with the 4 °C test temperature, this plastic response, (i.e., the acute thermal sensitivity of metabolic rate), was not different across populations. Surprisingly, we found that winter-acclimated urban ant populations exhibited higher heat tolerance compared with rural ant populations, and that the magnitude of divergence was comparable to that observed among growing-season acclimated ants. Finally, we found no evidence of differences between populations with respect to changes in colony size from the beginning to the end of the overwintering experiment. Together, these findings indicate that despite the evolution of higher heat tolerance that is often accompanied by losses in low-temperature tolerance, urban acorn ants have retained several components of low-temperature physiological performance when assessed under ecologically relevant overwintering conditions. Our study suggests the importance of measuring physiological traits under seasonally-relevant conditions to understand the causes and consequences of evolutionary responses to contemporary warming.

Urban insect bioarks of the 21st century.

Insects exhibit divergent biodiversity responses to cities. Many urban populations are not at equilibrium: biodiversity decline or recovery from environmental perturbation is often still in progress. Substantial variation in urban biodiversity patterns suggests the need to understand its mechanistic basis. In addition, current urban infrastructure decisions might profoundly influence future biodiversity trends. Although many nature-based solutions to urban climate problems also support urban insect biodiversity, trade-offs are possible and should be avoided to maximize biodiversity-climate cobenefits. Because insects are coping with the dual threats of urbanization and climate change, there is an urgent need to design cities that facilitate persistence within the city footprint or facilitate compensatory responses to global climate change as species transit through the city footprint.

Vulnerability to climate change increases with trophic level in terrestrial organisms.

The resilience of ecosystem function under global climate change is governed by individual species vulnerabilities and the functional groups they contribute to (e.g. decomposition, primary production, pollination, primary, secondary and tertiary consumption). Yet it remains unclear whether species that contribute to different functional groups, which underpin ecosystem function, differ in their vulnerability to climate change. We used existing upper thermal limit data across a range of terrestrial species (N = 1701) to calculate species warming margins (degrees distance between a species upper thermal limit and the maximum environmental temperature they inhabit), as a metric of climate change vulnerability. We examined whether species that comprise different functional groups exhibit differential vulnerability to climate change, and if vulnerability trends change across geographic space while considering evolutionary history. Primary producers had the broadest warming margins across the globe (µ = 18.72 °C) and tertiary consumers had the narrowest warming margins (µ = 9.64 °C), where vulnerability tended to increase with trophic level. Warming margins had a nonlinear relationship (second-degree polynomial) with absolute latitude, where warming margins were narrowest at about 33°, and were broader at lower and higher absolute latitudes. Evolutionary history explained significant variation in species warming margins, as did the methodology used to estimate species upper thermal limits. We investigated if variation in body mass across the trophic levels could explain why higher trophic level organisms had narrower warming margins than lower trophic level organisms, however, we did not find support for this hypothesis. This study provides a critical first step in linking individual species vulnerabilities with whole ecosystem responses to climate change.

A global horizon scan for urban evolutionary ecology.

Research on the evolutionary ecology of urban areas reveals how human-induced evolutionary changes affect biodiversity and essential ecosystem services. In a rapidly urbanizing world imposing many selective pressures, a time-sensitive goal is to identify the emergent issues and research priorities that affect the ecology and evolution of species within cities. Here, we report the results of a horizon scan of research questions in urban evolutionary ecology submitted by 100 interdisciplinary scholars. We identified 30 top questions organized into six themes that highlight priorities for future research. These research questions will require methodological advances and interdisciplinary collaborations, with continued revision as the field of urban evolutionary ecology expands with the rapid growth of cities.

The importance of eco-evolutionary dynamics for predicting and managing insect range shifts.

Evolutionary change impacts the rate at which insect pests, pollinators, or disease vectors expand or contract their geographic ranges. Although evolutionary changes, and their ecological feedbacks, strongly affect these risks and associated ecological and economic consequences, they are often underappreciated in management efforts. Greater rigor and scope in study design, coupled with innovative technologies and approaches, facilitates our understanding of the causes and consequences of eco-evolutionary dynamics in insect range shifts. Future efforts need to ensure that forecasts allow for demographic and evolutionary change and that management strategies will maximize (or minimize) the adaptive potential of range-shifting insects, with benefits for biodiversity and ecosystem services.

Adaptation to Urban Heat Islands Enhances Thermal Performance Following Development under Chronic Thermal Stress but Not Benign Conditions in the Terrestrial Isopod Oniscus asellus.

AbstractThe effects of chronic thermal stress during development on thermal performance traits are not well characterized under urban heat islands, despite these conditions being biologically relevant for how organisms experience the urban environment and the often strong linkages between thermal performance traits and fitness. Here we use the terrestrial isopod Oniscus asellus to examine the effects of chronic thermal stress during development on voluntary running speed of urban and rural isopods. We used a laboratory common-garden experiment design with two developmental acclimation temperature treatments (21°C, a benign treatment, and 29°C, a stressful treatment) and three test temperatures (19°C, 31°C, 40°C); we tested running speed of individuals from urban and rural populations under each of the temperature combinations. We found that for both urban and rural isopods, running speed across three test temperatures was reduced under developmental acclimation conditions of 29°C compared with 21°C. Importantly, however, urban isopods had a running speed advantage over the rural isopods under the 29°C developmental acclimation conditions at the lower two test temperatures. No population differences were detected under benign developmental acclimation conditions of 21°C. The evolution of higher heat tolerance in urban isopods further supported the interpretation of adaptation to heat stress. Convergence of urban and rural isopod running speed at the highest test temperature, however, suggests potential limits or constraints on adaptation. Our results indicate that thermal adaptation to urban heat islands can mitigate negative effects of chronic developmental thermal stress, even when overall performance is reduced compared with benign conditions.

Adaptation to urban environments.

Despite widespread evidence of urban evolution, the adaptive nature of these changes is often unclear. We review different phenotypic and molecular lines of evidence used for assessing urban adaptation, discussing the benefits and limitations of each approach, and rare examples of their integration. We then provide a synthesis of local adaptation to urban and rural environments. These data were drawn from phenotypic reciprocal transplant studies, the majority of which focus on insects and other arthropods. Broadly, we found support for local adaptation to urban and rural environments. However, there was asymmetry in the evidence for local adaptation depending on population of origin, with urban adaptation being less prevalent than rural adaptation, suggesting many urban populations are still adapting to urban environments. Further, the general patterns were underlain by considerable variation among study systems; we discuss how environmental heterogeneity and costs of adaptation might explain system-specific variation in urban-rural local adaptation. We then look to the future of urban adaptation research, considering the magnitude and direction of adaptation in context of different agents of selection including urban heat islands, chemical pollutants, and biotic interactions.

In a nutshell, a reciprocal transplant experiment reveals local adaptation and fitness trade-offs in response to urban evolution in an acorn-dwelling ant.

Urban-driven evolution is widely evident, but whether these changes confer fitness benefits and thus represent adaptive urban evolution is less clear. We performed a multiyear field reciprocal transplant experiment of acorn-dwelling ants across urban and rural environments. Fitness responses were consistent with local adaptation: we found a survival advantage of the "home" and "local" treatments compared to "away" and "foreign" treatments. Seasonal bias in survival was consistent with evolutionary patterns of gains and losses in thermal tolerance traits across the urbanization gradient. Rural ants in the urban environment were more vulnerable in the summer, putatively due to low heat tolerance, and urban ants in the rural environment were more vulnerable in winter, putatively due to an evolved loss of cold tolerance. The results for fitness via fecundity were also generally consistent with local adaptation, if somewhat more complex. Urban-origin ants produced more alates in their home versus away environment, and rural-origin ants had a local advantage in the rural environment. Overall, the magnitude of local adaptation was lower for urban ants in the novel urban environment compared with rural ants adapted to the ancestral rural environment, adding further evidence that species might not keep pace with anthropogenic change.

Physiological adaptation to cities as a proxy to forecast global-scale responses to climate change.

Cities are emerging as a new venue to overcome the challenges of obtaining data on compensatory responses to climatic warming through phenotypic plasticity and evolutionary change. In this Review, we highlight how cities can be used to explore physiological trait responses to experimental warming, and also how cities can be used as human-made space-for-time substitutions. We assessed the current literature and found evidence for significant plasticity and evolution in thermal tolerance trait responses to urban heat islands. For those studies that reported both plastic and evolved components of thermal tolerance, we found evidence that both mechanisms contributed to phenotypic shifts in thermal tolerance, rather than plastic responses precluding or limiting evolved responses. Interestingly though, for a broader range of studies, we found that the magnitude of evolved shifts in thermal tolerance was not significantly different from the magnitude of shift in those studies that only reported phenotypic results, which could be a product of evolution, plasticity, or both. Regardless, the magnitude of shifts in urban thermal tolerance phenotypes was comparable to more traditional space-for-time substitutions across latitudinal and altitudinal clines in environmental temperature. We conclude by considering how urban-derived estimates of plasticity and evolution of thermal tolerance traits can be used to improve forecasting methods, including macrophysiological models and species distribution modelling approaches. Finally, we consider areas for further exploration including sub-lethal performance traits and thermal performance curves, assessing the adaptive nature of trait shifts, and taking full advantage of the environmental thermal variation that cities generate.

Evidence for the evolution of thermal tolerance, but not desiccation tolerance, in response to hotter, drier city conditions in a cosmopolitan, terrestrial isopod.

Cities are often hotter and drier compared with nearby undeveloped areas, but how organisms respond to these multifarious stressors associated with urban heat islands is largely unknown. Terrestrial isopods are especially susceptible to temperature and aridity stress as they have retained highly permeable gills from their aquatic ancestors. We performed a two temperature common garden experiment with urban and rural populations of the terrestrial isopod, Oniscus asellus, to uncover evidence for plastic and evolutionary responses to urban heat islands. We focused on physiological tolerance traits including tolerance of heat, cold, and desiccation. We also examined body size responses to urban heat islands, as size can modulate physiological tolerances. We found that different mechanisms underlie responses to urban heat islands. While evidence suggests urban isopods may have evolved higher heat tolerance, urban and rural isopods had statistically indistinguishable cold and desiccation tolerances. In both populations, plasticity to warmer rearing temperature diminished cold tolerance. Although field-collected urban and rural isopods were the same size, rearing temperature positively affected body size. Finally, larger size improved desiccation tolerance, which itself was influenced by rearing temperature. Our study demonstrates how multifarious changes associated with urban heat islands will not necessarily contribute to contemporary evolution in each of the corresponding physiological traits.

Pedal to the metal: Cities power evolutionary divergence by accelerating metabolic rate and locomotor performance.

Metabolic rates of ectotherms are expected to increase with global trends of climatic warming. But the potential for rapid, compensatory evolution of lower metabolic rate in response to rising temperatures is only starting to be explored. Here, we explored rapid evolution of metabolic rate and locomotor performance in acorn-dwelling ants (Temnothorax curvispinosus) in response to urban heat island effects. We reared ant colonies within a laboratory common garden (25°C) to generate a laboratory-born cohort of workers and tested their acute plastic responses to temperature. Contrary to expectations, urban ants exhibited a higher metabolic rate compared with rural ants when tested at 25°C, suggesting a potentially maladaptive evolutionary response to urbanization. Urban and rural ants had similar metabolic rates when tested at 38°C, as a consequence of a diminished plastic response of the urban ants. Locomotor performance also evolved such that the running speed of urban ants was faster than rural ants under warmer test temperatures (32°C and 42°C) but slower under a cooler test temperature (22°C). The resulting specialist-generalist trade-off and higher thermal optimum for locomotor performance might compensate for evolved increases in metabolic rate by allowing workers to more quickly scout and retrieve resources.

Socio-eco-evolutionary dynamics in cities.

Cities are uniquely complex systems regulated by interactions and feedbacks between nature and human society. Characteristics of human society-including culture, economics, technology and politics-underlie social patterns and activity, creating a heterogeneous environment that can influence and be influenced by both ecological and evolutionary processes. Increasing research on urban ecology and evolutionary biology has coincided with growing interest in eco-evolutionary dynamics, which encompasses the interactions and reciprocal feedbacks between evolution and ecology. Research on both urban evolutionary biology and eco-evolutionary dynamics frequently focuses on contemporary evolution of species that have potentially substantial ecological-and even social-significance. Still, little work fully integrates urban evolutionary biology and eco-evolutionary dynamics, and rarely do researchers in either of these fields fully consider the role of human social patterns and processes. Because cities are fundamentally regulated by human activities, are inherently interconnected and are frequently undergoing social and economic transformation, they represent an opportunity for ecologists and evolutionary biologists to study urban "socio-eco-evolutionary dynamics." Through this new framework, we encourage researchers of urban ecology and evolution to fully integrate human social drivers and feedbacks to increase understanding and conservation of ecosystems, their functions and their contributions to people within and outside cities.

Adaptive Evolution in Cities: Progress and Misconceptions.

Current narratives suggest that urban adaptation - the adaptive evolution of organisms to cities - is pervasive across taxa and cities. However, in reviewing hundreds of studies, we find only six comprehensive examples of species adaptively evolving to urbanization. We discuss the utility and shortcomings of methods for studying urban adaptation. We then review diverse systems offering preliminary evidence for urban adaptation and outline a research program for advancing its study. Urban environments constitute diverse, interacting selective agents that test the limits of adaptation. Understanding urban adaptation therefore offers unique opportunities for addressing fundamental questions in evolutionary biology and for better conserving biodiversity in cities. However, capitalizing on these opportunities requires appropriate research methods and dissemination of accurate narratives.

Evolution is a double-edged sword, not a silver bullet, to confront global change.

Although there is considerable optimism surrounding adaptive evolutionary responses to global change, relatively little attention has been paid to maladaptation in this context. In this review, we consider how global change might lead populations to become maladapted. We further consider how populations can evolve to new optima, fail to evolve and therefore remain maladapted, or become further maladapted through trait-driven or eco-evo-driven mechanisms after being displaced from their fitness optima. Our goal is to stimulate thinking about evolution as a "double-edged sword" that comprises both adaptive and maladaptive responses, rather than as a "silver bullet" or a purely adaptive mechanism to combat global change. We conclude by discussing how a better appreciation of environmentally driven maladaptation and maladaptive responses might improve our current understanding of population responses to global change and our ability to forecast future responses.

Remarkable insensitivity of acorn ant morphology to temperature decouples the evolution of physiological tolerance from body size under urban heat islands.

Environmental temperature can alter body size and thermal tolerance, yet the effects of temperature rise on the size-tolerance relationship remain unclear. Terrestrial ectotherms with larger body sizes typically exhibit greater tolerance of high (and low) temperatures. However, while warming tends to increase tolerance of high temperatures through phenotypic plasticity and evolutionary change, warming tends to decrease body size through these mechanisms and thus might indirectly contribute to worse tolerance of high temperatures. These contrasting effects of warming on body size, thermal tolerance, and their relationship are increasingly important in light of global climate change. Here, we used replicated urban heat islands to explore the size-tolerance relationship in response to warming. We performed a common garden experiment with a small acorn-dwelling ant species collected from urban and rural populations across three different cities and reared under five laboratory rearing temperatures from 21 to 29 °C. We found that acorn ant body size was remarkably insensitive to laboratory rearing temperature (ant workers exhibited no phenotypic plasticity in body size across rearing temperature) and among populations experiencing cooler rural versus warmer urban environmental temperatures (no evolved differences in body size between urban and rural populations). Further, this insensitivity of body size to temperature was highly consistent across each of the three cities we examined. Because body size was robust to temperature variation, previously described plastic and evolved shifts in heat (and cold) tolerance in acorn ant responses to urbanization were shown to be independent of shifts in body size. Indeed, genetic (colony-level) correlations between heat and cold tolerance traits and body size revealed no significant association between size and tolerance. Our results show how typical trait correlations, such as between size and thermal tolerance, might be decoupled as populations respond to contemporary environmental change.