Evidence for parallel adaptation to climate across the natural range of Arabidopsis thaliana

How organisms adapt to different climate habitats is a key question in evolutionary ecology and biological conservation. Species distributions are often determined by climate suitability. Consequently, the anthropogenic impact on earth's climate is of key concern to conservation efforts because of our relatively poor understanding of the ability of populations to track and evolve to climate change. Here, we investigate the ability of Arabidopsis thaliana to occupy climate space by quantifying the extent to which different climate regimes are accessible to different A. thaliana genotypes using publicly available data from a large‐scale genotyping project and from a worldwide climate database. The genetic distance calculated from 149 single‐nucleotide polymorphisms (SNPs) among 60 lineages of A. thaliana was compared to the corresponding climate distance among collection localities calculated from nine different climatic factors. A. thaliana was found to be highly labile when adapting to novel climate space, suggesting that populations may experience few constraints when adapting to changing climates. Our results also provide evidence of a parallel or convergent evolution on the molecular level supporting recent generalizations regarding the genetics of adaptation.     

Physiological constraints on organismal response to global warming: Mechanistic insights from clinally varying populations and implications for assessing endangerment

Recent syntheses indicate that global warming affects diverse biological processes, but also highlight the potential for some species to adapt behaviourally or evolutionarily to rapid climate change. Far less attention has addressed the alternative, that organisms lacking this ability may face extinction, a fate projected to befall one-quarter of global biodiversity. This conclusion is controversial, in part because there exist few mechanistic studies that show how climate change could precipitate extinction. We provide a concrete, mechanistic example of warming as a stressor of organisms that are closely adapted to cool climates from a comparative analysis of organismal tolerance among clinally varying populations along a natural thermal gradient. We found that two montane salamanders exhibit significant metabolic depression at temperatures within the natural thermal range experienced by low and middle elevation populations. Moreover, the magnitude of depression was inversely related to native elevation, suggesting that low elevation populations are already living near the limit of their physiological tolerances. If this finding generally applies to other montane specialists, the prognosis for biodiversity loss in typically diverse montane systems is sobering. We propose that indices of warming-induced stress tolerance may provide a critical new tool for quantitative assessments of endangerment due to anthropogenic climate change across diverse species.     

Biological responses to environmental heterogeneity under future ocean conditions

Organisms are projected to face unprecedented rates of change in future ocean conditions due to anthropogenic climate‐change. At present, marine life encounters a wide range of environmental heterogeneity from natural fluctuations to mean climate change. Manipulation studies suggest that biota from more variable marine environments have more phenotypic plasticity to tolerate environmental heterogeneity. Here, we consider current strategies employed by a range of representative organisms across various habitats – from short‐lived phytoplankton to long‐lived corals – in response to environmental heterogeneity. We then discuss how, if and when organismal responses (acclimate/migrate/adapt) may be altered by shifts in the magnitude of the mean climate‐change signal relative to that for natural fluctuations projected for coming decades. The findings from both novel climate‐change modelling simulations and prior biological manipulation studies, in which natural fluctuations are superimposed on those of mean change, provide valuable insights into organismal responses to environmental heterogeneity. Manipulations reveal that different experimental outcomes are evident between climate‐change treatments which include natural fluctuations vs. those which do not. Modelling simulations project that the magnitude of climate variability, along with mean climate change, will increase in coming decades, and hence environmental heterogeneity will increase, illustrating the need for more realistic biological manipulation experiments that include natural fluctuations. However, simulations also strongly suggest that the timescales over which the mean climate‐change signature will become dominant, relative to natural fluctuations, will vary for individual properties, being most rapid for CO₂ (~10 years from present day) to 4 decades for nutrients. We conclude that the strategies used by biota to respond to shifts in environmental heterogeneity may be complex, as they will have to physiologically straddle wide‐ranging timescales in the alteration of ocean conditions, including the need to adapt to rapidly rising CO₂ and also acclimate to environmental heterogeneity in more slowly changing properties such as warming.     

Complex life cycles and the responses of insects to climate change

Many organisms have complex life cycles with distinct life stages that experience different environmental conditions. How does the complexity of life cycles affect the ecological and evolutionary responses of organisms to climate change? We address this question by exploring several recent case studies and synthetic analyses of insects. First, different life stages may inhabit different microhabitats, and may differ in their thermal sensitivities and other traits that are important for responses to climate. For example, the life stages of Manduca experience different patterns of thermal and hydric variability, and differ in tolerance to high temperatures. Second, life stages may differ in their mechanisms for adaptation to local climatic conditions. For example, in Colias, larvae in different geographic populations and species adapt to local climate via differences in optimal and maximal temperatures for feeding and growth, whereas adults adapt via differences in melanin of the wings and in other morphological traits. Third, we extend a recent analysis of the temperature-dependence of insect population growth to demonstrate how changes in temperature can differently impact juvenile survival and adult reproduction. In both temperate and tropical regions, high rates of adult reproduction in a given environment may not be realized if occasional, high temperatures prevent survival to maturity. This suggests that considering the differing responses of multiple life stages is essential to understand the ecological and evolutionary consequences of climate change.     

Evolution under changing climates: climatic niche stasis despite rapid evolution in a non-native plant

A topic of great current interest is the capacity of populations to adapt genetically to rapidly changing climates, for example by evolving the timing of life-history events, but this is challenging to address experimentally. I use a plant invasion as a model system to tackle this question by combining molecular markers, a common garden experiment and climatic niche modelling. This approach reveals that non-native Lactuca serriola originates primarily from Europe, a climatic subset of its native range, with low rates of admixture from Asia. It has rapidly refilled its climatic niche in the new range, associated with the evolution of flowering phenology to produce clines along climate gradients that mirror those across the native range. Consequently, some non-native plants have evolved development times and grow under climates more extreme than those found in Europe, but not among populations from the native range as a whole. This suggests that many plant populations can adapt rapidly to changed climatic conditions that are already within the climatic niche space occupied by the species elsewhere in its range, but that evolution to conditions outside of this range is more difficult. These findings can also help to explain the prevalence of niche conservatism among non-native species.     

Microbially mediated climate feedbacks from wetland ecosystems

Wetlands are crucial nodes in the carbon cycle, emitting approximately 20% of global CH₄ while also sequestering 20%–30% of all soil carbon. Both greenhouse gas fluxes and carbon storage are driven by microbial communities in wetland soils. However, these key players are often overlooked or overly simplified in current global climate models. Here, we first integrate microbial metabolisms with biological, chemical, and physical processes occurring at scales from individual microbial cells to ecosystems. This conceptual scale-bridging framework guides the development of feedback loops describing how wetland-specific climate impacts (i.e., sea level rise in estuarine wetlands, droughts and floods in inland wetlands) will affect future climate trajectories. These feedback loops highlight knowledge gaps that need to be addressed to develop predictive models of future climates capturing microbial contributions. We propose a roadmap connecting environmental scientific disciplines to address these knowledge gaps and improve the representation of microbial processes in climate models. Together, this paves the way to understand how microbially mediated climate feedbacks from wetlands will impact future climate change.     

Challenging claims in the study of migratory birds and climate change

Recent shifts in phenology in response to climate change are well established but often poorly understood. Many animals integrate climate change across a spatially and temporally dispersed annual life cycle, and effects are modulated by ecological interactions, evolutionary change and endogenous control mechanisms. Here we assess and discuss key statements emerging from the rapidly developing study of changing spring phenology in migratory birds. These well‐studied organisms have been instrumental for understanding climate‐change effects, but research is developing rapidly and there is a need to attack the big issues rather than risking affirmative science. Although we agree poorly on the support for most claims, agreement regarding the knowledge basis enables consensus regarding broad patterns and likely causes. Empirical data needed for disentangling mechanisms are still scarce, and consequences at a population level and on community composition remain unclear. With increasing knowledge, the overall support (‘consensus view’) for a claim increased and between‐researcher variability in support (‘expert opinions') decreased, indicating the importance of assessing and communicating the knowledge basis. A proper integration across biological disciplines seems essential for the field's transition from affirming patterns to understanding mechanisms and making robust predictions regarding future consequences of shifting phenologies.     

Developmental bias in horned dung beetles and its contributions to innovation,adaptation, and resilience

Developmental processes transduce diverse influences during phenotype formation, thereby biasing and structuring amount and type of phenotypic variation available for evolutionary processes to act on. The causes, extent, and consequences of this bias are subject to significant debate. Here we explore the role of developmental bias in contributing to organisms’ ability to innovate, to adapt to novel or stressful conditions, and to generate well integrated, resilient phenotypes in the face of perturbations. We focus our inquiry on one taxon, the horned dung beetle genus Onthophagus, and review the role developmental bias might play across several levels of biological organization: (a) gene regulatory networks that pattern specific body regions; (b) plastic developmental mechanisms that coordinate body wide responses to changing environments and; (c) developmental symbioses and niche construction that enable organisms to build teams and to actively modify their own selective environments. We posit that across all these levels developmental bias shapes the way living systems innovate, adapt, and withstand stress, in ways that can alternately limit, bias, or facilitate developmental evolution. We conclude that the structuring contribution of developmental bias in evolution deserves further study to better understand why and how developmental evolution unfolds the way it does.     

Adaptation of <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis> to the Yangtze River basin

Background

Organisms need to adapt to keep pace with a changing environment. Examining recent range expansion aids our understanding of how organisms evolve to overcome environmental constraints. However, how organisms adapt to climate changes is a crucial biological question that is still largely unanswered. The plant Arabidopsis thaliana is an excellent system to study this fundamental question. Its origin is in the Iberian Peninsula and North Africa, but it has spread to the Far East, including the most south-eastern edge of its native habitats, the Yangtze River basin, where the climate is very different.

Results

We sequenced 118 A. thaliana strains from the region surrounding the Yangtze River basin. We found that the Yangtze River basin population is a unique population and diverged about 61,409 years ago, with gene flows occurring at two different time points, followed by a population dispersion into the Yangtze River basin in the last few thousands of years. Positive selection analyses revealed that biological regulation processes, such as flowering time, immune and defense response processes could be correlated with the adaptation event. In particular, we found that the flowering time gene SVP has contributed to A. thaliana adaptation to the Yangtze River basin based on genetic mapping.

Conclusions

A. thaliana adapted to the Yangtze River basin habitat by promoting the onset of flowering, a finding that sheds light on how a species can adapt to locales with very different climates.

     

Disciplinary reporting affects the interpretation of climate change impacts in global oceans

Climate change is affecting marine ecosystems, but different investigative approaches in physical, chemical, and biological disciplines may influence interpretations of climate‐driven changes in the ocean. Here, we review the ocean change literature from 2007 to 2012 based on 461 of the most highly cited studies in physical and chemical oceanography and three biological subdisciplines. Using highly cited studies, we focus on research that has shaped recent discourse on climate‐driven ocean change. Our review identified significant differences in spatial and temporal scales of investigation among disciplines. Physical/chemical studies had a median duration of 29 years (n = 150) and covered the greatest study areas (median 1.41 × 10⁷ km², n = 148). Few biological studies were conducted over similar spatial and temporal scales (median 8 years, n = 215; median 302 km², n = 196), suggesting a more limited ability to separate climate‐related responses from natural variability. We linked physical/chemical and biological disciplines by tracking studies examining biological responses to changing ocean conditions. Of the 545 biological responses recorded, a single physical or chemical stressor was usually implicated as the cause (59%), with temperature as the most common primary stressor (44%). The most frequently studied biological responses were changes in physiology (31%) and population abundance (30%). Differences in disciplinary studies, as identified in this review, can ultimately influence how researchers interpret climate‐related impacts in marine systems. We identified research gaps and the need for more discourse in (1) the Indian and other Southern Hemisphere ocean basins; (2) research themes such as archaea, bacteria, viruses, mangroves, turtles, and ocean acidification; (3) physical and chemical stressors such as dissolved oxygen, salinity, and upwelling; and (4) adaptive responses of marine organisms to climate‐driven ocean change. Our findings reveal that highly cited biological studies are rarely conducted on scales that match those of physical and chemical studies. Rather, we suggest a need for measuring responses at biologically relevant scales.     

Biodiversity informatics: organizing and linking information across the spectrum of life

Biological knowledge can be inferred from three major levels of information: molecules, organisms and ecologies. Bioinformatics is an established field that has made significant advances in the development of systems and techniques to organize contemporary molecular data; biodiversity informatics is an emerging discipline that strives to develop methods to organize knowledge at the organismal level extending back to the earliest dates of recorded natural history. Furthermore, while bioinformatics studies generally focus on detailed examinations of key 'model' organisms, biodiversity informatics aims to develop over-arching hypotheses that span the entire tree of life. Biodiversity informatics is presented here as a discipline that unifies biological information from a range of contemporary and historical sources across the spectrum of life using organisms as the linking thread. The present review primarily focuses on the use of organism names as a universal metadata element to link and integrate biodiversity data across a range of data sources.     

The world is not flat: defining relevant thermal landscapes in the context of climate change

Although climates are rapidly changing on a global scale, these changes cannot easily be extrapolated to the local scales experienced by organisms. In fact, such generalizations might be quite problematic. For instance, models used to predict shifts in the ranges of species during climate change rarely incorporate data resolved to <1 km(2), although most organisms integrate climatic drivers at much smaller scales. Empirical studies alone suggest that the operative temperatures of many organisms vary by as much as 10-20 °C on a local scale, depending on vegetation, geology, and topography. Furthermore, this variation in abiotic factors ignores thermoregulatory behaviors that many animals use to balance heat loads. Through a set of simulations, we demonstrate how variability in elevational topography can attenuate the effects of warming climates. These simulations suggest that changing climates do not always impact organisms negatively. Importantly, these simulations involve well-known relationships in biophysical ecology that show how no two organisms experience the same climate in the same way. We suggest that, when coupled with thermoregulatory behavior, variation in topographic features can mask the acute effect of climate change in many cases.     

Genotypic variation in phenological plasticity: Reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost

Species faced with rapidly shifting environments must be able to move, adapt, or acclimate in order to survive. One mechanism to meet this challenge is phenotypic plasticity: altering phenotype in response to environmental change. Here, we investigated the magnitude, direction, and consequences of changes in two key phenology traits (fall bud set and spring bud flush) in a widespread riparian tree species, Populus fremontii. Using replicated genotypes from 16 populations from throughout the species’ thermal range, and reciprocal common gardens at hot, warm, and cool sites, we identified four major findings: (a) There are significant genetic (G), environmental (E), and GxE components of variation for both traits across three common gardens; (b) The magnitude of phenotypic plasticity is correlated with provenance climate, where trees from hotter, southern populations exhibited up to four times greater plasticity compared to the northern, frost‐adapted populations; (c) Phenological mismatches are correlated with higher mortality as the transfer distances between provenance and garden increase; and (d) The relationship between plasticity and survival depends not only on the magnitude and direction of environmental transfer, but also on the type of environmental stress (i.e., heat or freezing), and how particular traits have evolved in response to that stress. Trees transferred to warmer climates generally showed small to moderate shifts in an adaptive direction, a hopeful result for climate change. Trees experiencing cooler climates exhibited large, non‐adaptive changes, suggesting smaller transfer distances for assisted migration. This study is especially important as it deconstructs trait responses to environmental cues that are rapidly changing (e.g., temperature and spring onset) and those that are fixed (photoperiod), and that vary across the species’ range. Understanding the magnitude and adaptive nature of phenotypic plasticity of multiple traits responding to multiple environmental cues is key to guiding restoration management decisions as climate continues to change.     

Climate of origin affects tick (Ixodes ricinus) host-seeking behavior in response to temperature: implications for resilience to climate change?

Climate warming is changing distributions and phenologies of many organisms and may also impact on vectors of disease-causing pathogens. In Europe, the tick Ixodes ricinus is the primary vector of medically important pathogens (e.g., Borrelia burgdorferi sensu lato, the causative agent of Lyme borreliosis). How might climate change affect I. ricinus host-seeking behavior (questing)? We hypothesize that, in order to maximize survival, I. ricinus have adapted their questing in response to temperature in accordance with local climates. We predicted that ticks from cooler climates quest at cooler temperatures than those from warmer climates. This would suggest that I. ricinus can adapt and therefore have the potential to be resilient to climate change. I. ricinus were collected from a cline of climates using a latitudinal gradient (northeast Scotland, North Wales, South England, and central France). Under laboratory conditions, ticks were subjected to temperature increases of 1°C per day, from 6 to 15°C. The proportion of ticks questing was recorded five times per temperature (i.e., per day). The theoretical potential to quest was then estimated for each population over the year for future climate change projections. As predicted, more ticks from cooler climates quested at lower temperatures than did ticks from warmer climates. The proportion of ticks questing was strongly associated with key climate parameters from each location. Our projections, based on temperature alone, suggested that populations could advance their activity season by a month under climate change, which has implications for exposure periods of hosts to tick-borne pathogens. Our findings suggest that I. ricinus have adapted their behavior in response to climate, implying some potential to adapt to climate change. Predictive models of I. ricinus dynamics and disease risk over continental scales would benefit from knowledge of these differences between populations.     

Developmental phenotypic plasticity: Where ecology and evolution meet molecular biology

The plastic response of phenotypic traits to environmental change is a common research focus in several disciplines - from ecology and evolutionary biology to physiology and molecular genetics. The use of model systems such as the flowering plant Arabidopsis thaliana has facilitated a dialogue between developmental biologists asking how plasticity is controlled (proximate causes) and organismal biologists asking why plasticity exists (ultimate causes). Researchers studying ultimate causes and consequences are increasingly compelled to reject simplistic, ‘black box’ models, while those studying proximate causes and mechanisms are increasingly obliged to subject their interpretations to ecological ‘reality checks.’ We review the successful multidisciplinary efforts to understand the phytochrome-mediated shade-avoidance and light-seeking responses of flowering plants as a pertinent example of convergence between evolutionary and molecular biology. In this example, the two-way exchange between reductionist and holist camps has been essential to rapid and sustained progress. This should serve as a model for future collaborative efforts towards understanding the responses of organisms to their constantly changing environments.     

Grand challenges in organismal biology

A renaissance in organismal biology has been sparked by recent conceptual, theoretical, methodological, and computational advances in the life sciences, along with an unprecedented interdisciplinary integration with Mathematics, Engineering, and the physical sciences. Despite a decades-long trend toward reductionist approaches to biological problems, it is increasingly recognized that whole organisms play a central role in organizing and interpreting information from across the biological spectrum. Organisms represent the nexus where sub- and supra-organismal processes meet, and it is the performance of organisms within the environment that provides the material for natural selection. Here, we identify five "grand challenges" for future research in organismal biology. It is intended that these challenges will spark further discussion in the broader community and identify future research priorities, opportunities, and directions, which will ultimately help to guide the allocation of support for and training in organismal biology.     

The worldwide airline network and the dispersal of exotic species: 2007–2010

International air travel has played a significant role in driving recent increases in the rates of biological invasion and spread of infectious diseases. By providing high speed, busy transport links between spatially distant, but climatically similar regions of the world, the worldwide airline network (WAN) increases the risks of deliberate or accidental movements and establishment of climatically sensitive exotic organisms. With traffic levels continuing to rise and climates changing regionally, these risks will vary, both seasonally and year-by-year. Here, detailed estimates of air traffic trends and climate changes for the period 2007-2010 are used to examine the likely directions and magnitudes of changes in climatically sensitive organism invasion risk across the WAN. Analysis of over 144 million flights from 2007-2010 shows that by 2010, the WAN is likely to change little overall in terms of connecting regions with similar climates, but anticipated increases in traffic and local variations in climatic changes should increase the risks of exotic species movement on the WAN and establishment in new areas. These overall shifts mask spatially and temporally heterogenous changes across the WAN, where, for example, traffic increases and climatic convergence by July 2010 between parts of China and northern Europe and North America raise the likelihood of exotic species invasions, whereas anticipated climatic shifts may actually reduce invasion risks into much of eastern Europe.     

The combined effects of reactant kinetics and enzyme stability explain the temperature dependence of metabolic rates

A mechanistic understanding of the response of metabolic rate to temperature is essential for understanding thermal ecology and metabolic adaptation. Although the Arrhenius equation has been used to describe the effects of temperature on reaction rates and metabolic traits, it does not adequately describe two aspects of the thermal performance curve (TPC) for metabolic rate—that metabolic rate is a unimodal function of temperature often with maximal values in the biologically relevant temperature range and that activation energies are temperature dependent. We show that the temperature dependence of metabolic rate in ectotherms is well described by an enzyme‐assisted Arrhenius (EAAR) model that accounts for the temperature‐dependent contribution of enzymes to decreasing the activation energy required for reactions to occur. The model is mechanistically derived using the thermodynamic rules that govern protein stability. We contrast our model with other unimodal functions that also can be used to describe the temperature dependence of metabolic rate to show how the EAAR model provides an important advance over previous work. We fit the EAAR model to metabolic rate data for a variety of taxa to demonstrate the model's utility in describing metabolic rate TPCs while revealing significant differences in thermodynamic properties across species and acclimation temperatures. Our model advances our ability to understand the metabolic and ecological consequences of increases in the mean and variance of temperature associated with global climate change. In addition, the model suggests avenues by which organisms can acclimate and adapt to changing thermal environments. Furthermore, the parameters in the EAAR model generate links between organismal level performance and underlying molecular processes that can be tested for in future work.     

Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community‐level responses

Biological communities are shaped by complex interactions between organisms and their environment as well as interactions with other species. Humans are rapidly changing the marine environment through increasing greenhouse gas emissions, resulting in ocean warming and acidification. The first response by animals to environmental change is predominantly through modification of their behaviour, which in turn affects species interactions and ecological processes. Yet, many climate change studies ignore animal behaviour. Furthermore, our current knowledge of how global change alters animal behaviour is mostly restricted to single species, life phases and stressors, leading to an incomplete view of how coinciding climate stressors can affect the ecological interactions that structure biological communities. Here, we first review studies on the effects of warming and acidification on the behaviour of marine animals. We demonstrate how pervasive the effects of global change are on a wide range of critical behaviours that determine the persistence of species and their success in ecological communities. We then evaluate several approaches to studying the ecological effects of warming and acidification, and identify knowledge gaps that need to be filled, to better understand how global change will affect marine populations and communities through altered animal behaviours. Our review provides a synthesis of the far‐reaching consequences that behavioural changes could have for marine ecosystems in a rapidly changing environment. Without considering the pervasive effects of climate change on animal behaviour we will limit our ability to forecast the impacts of ocean change and provide insights that can aid management strategies.     

Introduction. Integration of ecology and endocrinology in avian reproduction: a new synthesis

Birds are some of the most familiar organisms of global ecosystems. Changes in the visibility and abundance of birds are therefore excellent indicators of population and physiological responses to habitat changes and are a major focus for public concern about detrimental environmental changes. In order to understand how birds respond to these challenges, it is essential to determine how the environment affects reproduction under natural conditions. The continuum from environmental variables (cues) to reproductive life-history traits depends upon a cascade of neural and physiological processes that determine the extent and rate at which birds will be able to adapt to changes in their environment. For a full understanding of this ability to adapt, ecologists and endocrinologists need to collaborate and build a common framework. The objective of this theme issue is to bring together a series of papers addressing how evolutionary ecologists and endocrinologists can collaborate directly using avian reproduction as a model system. First, we address the need to integrate ecology and endocrinology and what benefits to biological knowledge will be gained. The papers collected in this issue represent a new synthesis of ecology and endocrinology as discussed in three E-BIRD workshops. The three main foci are trade-offs and constraints, maternal effects and individual variation. Authors within each group present ecological and endocrinological aspects of their topics and many go on to outline testable hypotheses. Finally, we discuss where the major problems remain and how this issue points out where these need collaborative efforts of ecologists and endocrinologists. Specific challenges are raised to future researchers to break through intellectual barriers and explore new frontiers. This framework of topics will ultimately apply to all taxa because the principles involved are universal and hopefully will have direct application to programmes integrating organisms and genes throughout biological sciences.