Non-climatic thermal adaptation: implications for species' responses to climate warming

There is considerable interest in understanding how ectothermic animals may physiologically and behaviourally buffer the effects of climate warming. Much less consideration is being given to how organisms might adapt to non-climatic heat sources in ways that could confound predictions for responses of species and communities to climate warming. Although adaptation to non-climatic heat sources (solar and geothermal) seems likely in some marine species, climate warming predictions for marine ectotherms are largely based on adaptation to climatically relevant heat sources (air or surface sea water temperature). Here, we show that non-climatic solar heating underlies thermal resistance adaptation in a rocky–eulittoral-fringe snail. Comparisons of the maximum temperatures of the air, the snail''s body and the rock substratum with solar irradiance and physiological performance show that the highest body temperature is primarily controlled by solar heating and re-radiation, and that the snail''s upper lethal temperature exceeds the highest climatically relevant regional air temperature by approximately 22°C. Non-climatic thermal adaptation probably features widely among marine and terrestrial ectotherms and because it could enable species to tolerate climatic rises in air temperature, it deserves more consideration in general and for inclusion into climate warming models.     

Cold truths: how winter drives responses of terrestrial organisms to climate change

Winter is a key driver of individual performance, community composition, and ecological interactions in terrestrial habitats. Although climate change research tends to focus on performance in the growing season, climate change is also modifying winter conditions rapidly. Changes to winter temperatures, the variability of winter conditions, and winter snow cover can interact to induce cold injury, alter energy and water balance, advance or retard phenology, and modify community interactions. Species vary in their susceptibility to these winter drivers, hampering efforts to predict biological responses to climate change. Existing frameworks for predicting the impacts of climate change do not incorporate the complexity of organismal responses to winter. Here, we synthesise organismal responses to winter climate change, and use this synthesis to build a framework to predict exposure and sensitivity to negative impacts. This framework can be used to estimate the vulnerability of species to winter climate change. We describe the importance of relationships between winter conditions and performance during the growing season in determining fitness, and demonstrate how summer and winter processes are linked. Incorporating winter into current models will require concerted effort from theoreticians and empiricists, and the expansion of current growing‐season studies to incorporate winter.     

A macroecological approach to evolutionary rescue and adaptation to climate change

Despite the widespread use of ecological niche models (ENMs) for predicting the responses of species to climate change, these models do not explicitly incorporate any population‐level mechanism. On the other hand, mechanistic models adding population processes (e.g. biotic interactions, dispersal and adaptive potential to abiotic conditions) are much more complex and difficult to parameterize, especially if the goal is to predict range shifts for many species simultaneously. In particular, the adaptive potential (based on genetic adaptations, phenotypic plasticity and behavioral adjustments for physiological responses) of local populations has been a less studied mechanism affecting species’ responses to climatic change so far. Here, we discuss and apply an alternative macroecological framework to evaluate the potential role of evolutionary rescue under climate change based on ENMs. We begin by reviewing eco‐evolutionary models that evaluate the maximum sustainable evolutionary rate under a scenario of environmental change, showing how they can be used to understand the impact of temperature change on a Neotropical anuran species, the Schneider's toad Rhinella diptycha. Then we show how to evaluate spatial patterns of species’ geographic range shift using such models, by estimating evolutionary rates at the trailing edge of species distribution estimated by ENMs and by recalculating the relative amount of total range loss under climate change. We show how different models can reduce the expected range loss predicted for the studied species by potential ecophysiological adaptations in some regions of the trailing edge predicted by ENMs. For general applications, we believe that parameters for large numbers of species and populations can be obtained from macroecological generalizations (e.g. allometric equations and ecogeographical rules), so our framework coupling ENMs with eco‐evolutionary models can be applied to achieve a more accurate picture of potential impacts from climate change and other threats to biodiversity.     

Rapid adaptation to climate change

In recent years, amid growing concerns that changing climate is affecting species distributions and ecosystems, predicting responses to rapid environmental change has become a major goal. In this issue, Franks and colleagues take a first step towards this objective (Franks et al. 2016). They examine genomewide signatures of selection in populations of Brassica rapa after a severe multiyear drought. Together with other authors, Franks had previously shown that flowering time was reduced after this particular drought and that the reduction was genetically encoded. Now, the authors have sequenced previously stored samples to compare allele frequencies before and after the drought and identify the loci with the most extreme shifts in frequencies. The loci they identify largely differ between populations, suggesting that different genetic variants may be responsible for reduction in flowering time in the two populations.     

Widespread parallel population adaptation to climate variation across a radiation: implications for adaptation to climate change

Global warming will impact species in a number of ways, and it is important to know the extent to which natural populations can adapt to anthropogenic climate change by natural selection. Parallel microevolution within separate species can demonstrate natural selection, but several studies of homoplasy have not yet revealed examples of widespread parallel evolution in a generic radiation. Taking into account primary phylogeographic divisions, we investigate numerous quantitative traits (size, shape, scalation, colour pattern and hue) in anole radiations from the mountainous Lesser Antillean islands. Adaptation to climatic differences can lead to very pronounced differences between spatially close populations with all studied traits showing some evidence of parallel evolution. Traits from shape, scalation, pattern and hue (particularly the latter) show widespread evolutionary parallels within these species in response to altitudinal climate variation greater than extreme anthropogenic climate change predicted for 2080. This gives strong evidence of the ability to adapt to climate variation by natural selection throughout this radiation. As anoles can evolve very rapidly, it suggests anthropogenic climate change is likely to be less of a conservation threat than other factors, such as habitat loss and invasive species, in this, Lesser Antillean, biodiversity hot spot.     

Population responses within a landscape matrix: a macrophysiological approach to understanding climate change impacts

Global environmental change (GEC) is a significant concern. However, forecasting the outcomes of this change for species and ecosystems remains a major challenge. In particular, predicting specific changes in systems where initial conditions, instabilities, and model errors have large impacts on the outcome is problematic. Indeed, predictive community ecology has been deemed unworthy of pursuit or an unreachable goal. However, new developments in large-scale biology provide ways of thinking that might substantially improve forecasts of local and regional impacts of climate change. Most notably, these are the explicit recognition of the regional and landscape contexts within which populations reside, the matrix approach that can be used to investigate the consequences of population variation across space and within assemblages, and the development of macrophysiology, which explicitly seeks to understand the ecological implications of physiological variation across large spatial and temporal scales. Here we explore how a combination of these approaches might promote further understanding and forecasting of the effects of global climate change and perhaps other GEC drivers on biodiversity. We focus on the population level, examining the ways in which environmental variation might be translated through performance and its plasticity to variation in demography.     

Bat responses to climate change: a systematic review

Understanding how species respond to climate change is key to informing vulnerability assessments and designing effective conservation strategies, yet research efforts on wildlife responses to climate change fail to deliver a representative overview due to inherent biases. Bats are a species-rich, globally distributed group of organisms that are thought to be particularly sensitive to the effects of climate change because of their high surface-to-volume ratios and low reproductive rates. We systematically reviewed the literature on bat responses to climate change to provide an overview of the current state of knowledge, identify research gaps and biases and highlight future research needs. We found that studies are geographically biased towards Europe, North America and Australia, and temperate and Mediterranean biomes, thus missing a substantial proportion of bat diversity and thermal responses. Less than half of the published studies provide concrete evidence for bat responses to climate change. For over a third of studied bat species, response evidence is only based on predictive species distribution models. Consequently, the most frequently reported responses involve range shifts (57% of species) and changes in patterns of species diversity (26%). Bats showed a variety of responses, including both positive (e.g. range expansion and population increase) and negative responses (range contraction and population decrease), although responses to extreme events were always negative or neutral. Spatial responses varied in their outcome and across families, with almost all taxonomic groups featuring both range expansions and contractions, while demographic responses were strongly biased towards negative outcomes, particularly among Pteropodidae and Molossidae. The commonly used correlative modelling approaches can be applied to many species, but do not provide mechanistic insight into behavioural, physiological, phenological or genetic responses. There was a paucity of experimental studies (26%), and only a small proportion of the 396 bat species covered in the examined studies were studied using long-term and/or experimental approaches (11%), even though they are more informative about the effects of climate change. We emphasise the need for more empirical studies to unravel the multifaceted nature of bats' responses to climate change and the need for standardised study designs that will enable synthesis and meta-analysis of the literature. Finally, we stress the importance of overcoming geographic and taxonomic disparities through strengthening research capacity in the Global South to provide a more comprehensive view of terrestrial biodiversity responses to climate change.     

Forest tree species adaptation to climate across biomes: Building on the legacy of ecological genetics to anticipate responses to climate change

Intraspecific variation plays a critical role in extant and future forest responses to climate change. Forest tree species with wide climatic niches rely on the intraspecific variation resulting from genetic adaptation and phenotypic plasticity to accommodate spatial and temporal climate variability. A centuries-old legacy of forest ecological genetics and provenance trials has provided a strong foundation upon which to continue building on this knowledge, which is critical to maintain climate-adapted forests. Our overall objective is to understand forest trees intraspecific responses to climate across species and biomes, while our specific objectives are to describe ecological genetics models used to build our foundational knowledge, summarize modeling approaches that have expanded the traditional toolset, and extensively review the literature from 1994 to 2021 to highlight the main contributions of this legacy and the new analyzes of provenance trials. We reviewed 103 studies comprising at least three common gardens, which covered 58 forest tree species, 28 of them with range-wide studies. Although studies using provenance trial data cover mostly commercially important forest tree species from temperate and boreal biomes, this synthesis provides a global overview of forest tree species adaptation to climate. We found that evidence for genetic adaptation to local climate is commonly present in the species studied (79%), being more common in conifers (87.5%) than in broadleaf species (67%). In 57% of the species, clines in fitness-related traits were associated with temperature variables, in 14% of the species with precipitation, and in 25% of the species with both. Evidence of adaptation lags was found in 50% of the species with range-wide studies. We conclude that ecological genetics models and analysis of provenance trial data provide excellent insights on intraspecific genetic variation, whereas the role and limits of phenotypic plasticity, which will likely determine the fate of extant forests, is vastly understudied.     

The role of industrial ecology in food and agriculture's adaptation to climate change

The food and agriculture sectors contribute significantly to climate change, but are also particularly vulnerable to its effects. Industrial ecology has robustly addressed these sectors’ contributions to climate change, but not their vulnerability to climate change. Climate change vulnerability must be addressed through development of climate change adaptation and resiliency strategies. However, there is a fundamental tension between the primary objectives of industrial ecology (efficiency, cyclic flows, and pollution prevention) and what is needed for climate change adaptation and resiliency. We develop here two potential ways through which the field can overcome (or work within) this tension and combine the tools and methods of industrial ecology with the science and process of climate change adaptation. The first layers industrial ecology tools on top of climate change adaptation strategies, allowing one to, for example, compare the environmental impacts of different adaptation strategies. The other embeds climate change adaptation and resiliency within industrial ecology tools, for example, by redefining the functional unit in life cycle assessment (LCA) to include functions of resiliency. In both, industrial ecology plays a somewhat narrow role, informing climate change adaptation and resilience decision‐making by providing quantitative indicators of environmental performance. This role for industrial ecology is important given the significant contributions and potential for mitigation of greenhouse gas emissions from food and agriculture. However, it suggests that industrial ecology's role in climate adaptation will be as an evaluator of adaptation strategies, rather than an originator.     

The dynamics and role of sphingolipids in eukaryotic organisms upon thermal adaptation

All living beings have an optimal temperature for growth and survival. With the advancement of global warming, the search for understanding adaptive processes to climate changes has gained prominence. In this context, all living beings monitor the external temperature and develop adaptive responses to thermal variations. These responses ultimately change the functioning of the cell and affect the most diverse structures and processes. One of the first structures to detect thermal variations is the plasma membrane, whose constitution allows triggering of intracellular signals that assist in the response to temperature stress. Although studies on this topic have been conducted, the underlying mechanisms of recognizing thermal changes and modifying cellular functioning to adapt to this condition are not fully understood. Recently, many reports have indicated the participation of sphingolipids (SLs), major components of the plasma membrane, in the regulation of the thermal stress response. SLs can structurally reinforce the membrane or/and send signals intracellularly to control numerous cellular processes, such as apoptosis, cytoskeleton polarization, cell cycle arresting and fungal virulence. In this review, we discuss how SLs synthesis changes during both heat and cold stresses, focusing on fungi, plants, animals and human cells. The role of lysophospholipids is also discussed.     

Pathogen adaptation to seasonal forcing and climate change

Many diverse infectious diseases exhibit seasonal dynamics. Seasonality in disease incidence has been attributed to seasonal changes in pathogen transmission rates, resulting from fluctuations in extrinsic climate factors. Multi-strain infectious diseases with strain-specific seasonal signatures, such as cholera, indicate that a range of seasonal patterns in transmission rates is possible in identical environments. We therefore consider pathogens capable of evolving their 'seasonal phenotype', a trait that determines the sensitivity of their transmission rates to environmental variability. We introduce a theoretical framework, based on adaptive dynamics, for predicting the evolution of disease dynamics in seasonal environments. Changes in the seasonality of environmental factors are one important avenue for the effects of climate change on disease. This model also provides a framework for examining these effects on pathogen evolution and associated disease dynamics. An application of this approach gives an explanation for the recent cholera strain replacement in Bangladesh, based on changes in monsoon rainfall patterns.     

Assisted colonization as a climate change adaptation tool

Assisted colonization is a form of conservation translocation which introduces species at risk from extinction to new habitats, beyond their current range, in anticipation of more suitable conditions. Identifying which species, communities and ecosystems may benefit most from assisted colonization in coming decades is a key goal for conservation. Climate change is expected to lead to the loss or movement of suitable habitat for a range of species and anticipating which can be effectively conserved through assisted colonization is critical. Here, we identify a series of scenarios that may predispose terrestrial species to the need for assisted colonization in order to reduce extinction risk resulting from anthropogenic climate change and assemble a list of traits commonly associated with at‐risk species. These traits may help to provide broad‐scale guidance on how to select species to target for assisted colonization as a conservation management response to climate change. We also identify six key themes associated with successful conservation translocations including recipient site selection and preparation, a clear understanding of species biology and ecology, and taking lessons from invasive species research.     

Potential for adaptation to climate change in a coral reef fish

Predicting the impacts of climate change requires knowledge of the potential to adapt to rising temperatures, which is unknown for most species. Adaptive potential may be especially important in tropical species that have narrow thermal ranges and live close to their thermal optimum. We used the animal model to estimate heritability, genotype by environment interactions and nongenetic maternal components of phenotypic variation in fitness‐related traits in the coral reef damselfish, Acanthochromis polyacanthus. Offspring of wild‐caught breeding pairs were reared for two generations at current‐day and two elevated temperature treatments (+1.5 and +3.0 °C) consistent with climate change projections. Length, weight, body condition and metabolic traits (resting and maximum metabolic rate and net aerobic scope) were measured at four stages of juvenile development. Additive genetic variation was low for length and weight at 0 and 15 days posthatching (dph), but increased significantly at 30 dph. By contrast, nongenetic maternal effects on length, weight and body condition were high at 0 and 15 dph and became weaker at 30 dph. Metabolic traits, including net aerobic scope, exhibited high heritability at 90 dph. Furthermore, significant genotype x environment interactions indicated potential for adaptation of maximum metabolic rate and net aerobic scope at higher temperatures. Net aerobic scope was negatively correlated with weight, indicating that any adaptation of metabolic traits at higher temperatures could be accompanied by a reduction in body size. Finally, estimated breeding values for metabolic traits in F2 offspring were significantly affected by the parental rearing environment. Breeding values at higher temperatures were highest for transgenerationally acclimated fish, suggesting a possible role for epigenetic mechanisms in adaptive responses of metabolic traits. These results indicate a high potential for adaptation of aerobic scope to higher temperatures, which could enable reef fish populations to maintain their performance as ocean temperatures rise.     

A field incubation approach to evaluate the depth dependence of soil biogeochemical responses to climate change

Soil biogeochemical processes may present depth-dependent responses to climate change, due to vertical environmental gradients (e.g., thermal and moisture regimes, and the quantity and quality of soil organic matter) along soil profile. However, it is a grand challenge to distinguish such depth dependence under field conditions. Here we present an innovative, cost-effective and simple approach of field incubation of intact soil cores to explore such depth dependence. The approach adopts field incubation of two sets of intact soil cores: one incubated right-side up (i.e., non-inverted), and another upside down (i.e., inverted). This inversion keeps soil intact but changes the depth of the soil layer of same depth origin. Combining reciprocal translocation experiments to generate natural climate shift, we applied this incubation approach along a 2200 m elevational mountainous transect in southeast Tibetan Plateau. We measured soil respiration (Rs) from non-inverted and inverted cores of 1 m deep, respectively, which were exchanged among and incubated at different elevations. The results indicated that Rs responds significantly (p < .05) to translocation-induced climate shifts, but this response is depth-independent. As the incubation proceeds, Rs from both non-inverted and inverted cores become more sensitive to climate shifts, indicating higher vulnerability of persistent soil organic matter (SOM) to climate change than labile components, if labile substrates are assumed to be depleted with the proceeding of incubation. These results show in situ evidence that whole-profile SOM mineralization is sensitive to climate change regardless of the depth location. Together with measurements of vertical physiochemical conditions, the inversion experiment can serve as an experimental platform to elucidate the depth dependence of the response of soil biogeochemical processes to climate change.