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.     

Reduced variability in range‐edge butterfly populations over three decades of climate warming

Populations at the high latitude edge of species’ geographical ranges are thought to show larger interannual population fluctuations, with subsequent higher local extinction risk, than those within the ‘core’ climatic range. As climate envelopes shift northward under climate warming, however, we would expect populations to show dampened variability. We test this hypothesis using annual abundance indices from 19 butterfly species across 79 British monitoring sites between 1976 and 2009, a period of climatic warming. We found that populations in the latter (warmer) half of the recording period show reduced interannual population variability. Species with more southerly European distributions showed the greatest dampening in population variability over time. Our results suggest that increases in population variability occur towards climatic range boundaries. British sites, previously existing at the margins of suitable climate space, now appear to fall closer to the core climatic range for many butterfly species.     

A genome‐wide search for local adaptation in a terrestrial‐breeding frog reveals vulnerability to climate change

Terrestrial‐breeding amphibians are likely to be vulnerable to warming and drying climates, as their embryos require consistent moisture for successful development. Adaptation to environmental change will depend on sufficient genetic variation existing within or between connected populations. Here, we use Single Nucleotide Polymorphism (SNP) data to investigate genome‐wide patterns in genetic diversity, gene flow and local adaptation in a terrestrial‐breeding frog (Pseudophryne guentheri) subject to a rapidly drying climate and recent habitat fragmentation. The species was sampled across 12 central and range‐edge populations (192 samples), and strong genetic structure was apparent, as were high inbreeding coefficients. Populations showed differences in genetic diversity, and one population lost significant genetic diversity in a decade. More than 500 SNP loci were putatively under directional selection, and 413 of these loci were correlated with environmental variables such as temperature, rainfall, evaporation and soil moisture. One locus showed homology to a gene involved in the activation of maturation in Xenopus oocytes, which may facilitate rapid development of embryos in drier climates. The low genetic diversity, strong population structuring and presence of local adaptation revealed in this study shows why management strategies such as targeted gene flow may be necessary to assist isolated populations to adapt to future climates.     

Similarities in butterfly emergence dates among populations suggest local adaptation to climate

Phenology shifts are the most widely cited examples of the biological impact of climate change, yet there are few assessments of potential effects on the fitness of individual organisms or the persistence of populations. Despite extensive evidence of climate‐driven advances in phenological events over recent decades, comparable patterns across species' geographic ranges have seldom been described. Even fewer studies have quantified concurrent spatial gradients and temporal trends between phenology and climate. Here we analyse a large data set (~129 000 phenology measures) over 37 years across the UK to provide the first phylogenetic comparative analysis of the relative roles of plasticity and local adaptation in generating spatial and temporal patterns in butterfly mean flight dates. Although populations of all species exhibit a plastic response to temperature, with adult emergence dates earlier in warmer years by an average of 6.4 days per °C, among‐population differences are significantly lower on average, at 4.3 days per °C. Emergence dates of most species are more synchronised over their geographic range than is predicted by their relationship between mean flight date and temperature over time, suggesting local adaptation. Biological traits of species only weakly explained the variation in differences between space‐temperature and time‐temperature phenological responses, suggesting that multiple mechanisms may operate to maintain local adaptation. As niche models assume constant relationships between occurrence and environmental conditions across a species' entire range, an important implication of the temperature‐mediated local adaptation detected here is that populations of insects are much more sensitive to future climate changes than current projections suggest.     

The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change

Species are the unit of analysis in many global change and conservation biology studies; however, species are not uniform entities but are composed of different, sometimes locally adapted, populations differing in plasticity. We examined how intraspecific variation in thermal niches and phenotypic plasticity will affect species distributions in a warming climate. We first developed a conceptual model linking plasticity and niche breadth, providing five alternative intraspecific scenarios that are consistent with existing literature. Secondly, we used ecological niche‐modeling techniques to quantify the impact of each intraspecific scenario on the distribution of a virtual species across a geographically realistic setting. Finally, we performed an analogous modeling exercise using real data on the climatic niches of different tree provenances. We show that when population differentiation is accounted for and dispersal is restricted, forecasts of species range shifts under climate change are even more pessimistic than those using the conventional assumption of homogeneously high plasticity across a species' range. Suitable population‐level data are not available for most species so identifying general patterns of population differentiation could fill this gap. However, the literature review revealed contrasting patterns among species, urging greater levels of integration among empirical, modeling and theoretical research on intraspecific phenotypic variation.     

Keeping up with a warming world; assessing the rate of adaptation to climate change

The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity.The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in a changing environment, and (iv) adaptation via immigration of individuals with genotypes adapted to warmer environments also involves microevolution as these genotypes are better adapted in terms of temperature, but not in terms of, for instance, photoperiod.Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions.Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.     

One stimulus—Two responses: Host and parasite life‐history variation in response to environmental stress

Climate change stressors will place different selective pressures on both parasites and their hosts, forcing individuals to modify their life‐history strategies and altering the distribution and prevalence of disease. Few studies have investigated whether parasites are able to respond to host stress and respond by varying their reproductive schedules. Additionally, multiple environmental stressors can limit the ability of a host to respond adaptively to parasite infection. This study compared both host and parasite life‐history parameters in unstressed and drought‐stressed environments using the human parasite, Schistosoma mansoni, in its freshwater snail intermediate host. Snail hosts infected with the parasite demonstrated a significant reproductive burst during the prepatent period (fecundity compensation), but that response was absent in a drought‐stressed environment. This is the first report of the elimination of host fecundity compensation to parasitism when exposed to additional environmental stress. More surprisingly, we found that infections in drought‐stressed snails had significantly higher parasite reproductive outputs than infections in unstressed snails. The finding suggests that climate change may alter the infection dynamics of this human parasite.     

Highlighting declines of cold‐demanding plant species in lowlands under climate warming

High rates of species extinction have been predicted for the next century as a consequence of climate change. Although species range shifts have been widely reported, evidence of changes in species frequency linked to recent climate change is scarce. Moreover, studies have mainly focused on mountainous ecosystems and species. There is thus a clear lack of understanding of the recent changes in species frequencies linked to climate change across their whole range. Using a large forest vegetation‐plot database, we investigated changes in cold and warm‐demanding forest plant species frequencies between the periods 1914–1987 and 1997–2013 in French lowlands and highlands. Changes in frequencies were assessed for 185 lowland (warm‐demanding), 135 sub‐montane (intermediate) and 104 montane (cold‐demanding) forest plant species. Observed changes were compared to predicted changes derived from species distribution model predictions. The frequency of montane and sub‐montane species strongly declined, whereas the frequency of lowland species remained steady in lowland areas. In highlands, the frequency of lowland, sub‐montane and montane species increased, remained steady and decreased, respectively. Predicted and observed trends of changes in the frequency of forest plant species were in agreement. These results clearly show that cold‐demanding species are currently declining in lowlands that correspond to their warm range margins, whereas warm‐demanding species are expanding in highlands that correspond to their cold range margins. These trends can be seen as early signs of future regional extinction and reshuffling of the spatial presence of species due to climate warming.     

Phenotypic plasticity closely linked to climate at origin and resulting in increased mortality under warming and frost stress in a common grass

Phenotypic plasticity is important for species responses to global change and species coexistence. Phenotypic plasticity differs among species and traits and changes across environments. Here, we investigated phenotypic plasticity of the widespread grass Arrhenatherum elatius in response to winter warming and frost stress by comparing phenotypic plasticity of 11 geographically and environmentally distinct populations of this species to phenotypic plasticity of populations of different species originating from a single environment. The variation in phenotypic plasticity was similar for populations of a single species from different locations compared to populations of functionally and taxonomically diverse species from one environment for the studied traits (leaf biomass production and root integrity after frost) across three indices of phenotypic plasticity (RDPI, PIN, slope of reaction norm). Phenotypic plasticity was not associated with neutral genetic diversity but closely linked to the climate of the populations’ origin. Populations originating from warmer and more variable climates showed higher phenotypic plasticity. This indicates that phenotypic plasticity can itself be considered as a trait subject to local adaptation to climate. Finally, our data emphasize that high phenotypic plasticity is not per se positive for adaptation to climate change, as differences in stress responses are resulting in high phenotypic plasticity as expressed by common plasticity indices, which is likely to be related to increased mortality under stress in more plastic populations.     

Climate adaptation is not enough: warming does not facilitate success of southern tundra plant populations in the high Arctic

Rapidly rising temperatures are expected to cause latitudinal and elevational range shifts as species track their optimal climate north and upward. However, a lack of adaptation to environmental conditions other than climate – for example photoperiod, biotic interactions, or edaphic conditions – might limit the success of immigrants in a new location despite hospitable climatic conditions. Here, we present one of the first direct experimental tests of the hypothesis that warmer temperatures at northern latitudes will confer a fitness advantage to southern immigrants relative to native populations. As rates of warming in the Arctic are more than double the global average, understanding the impacts of warming in Arctic ecosystems is especially urgent. We established experimentally warmed and nonwarmed common garden plots at Alexandra Fiord, Ellesmere Island in the Canadian High Arctic with seeds of two forb species (Oxyria digyna and Papaver radicatum) originating from three to five populations at different latitudes across the Arctic. We found that plants from the local populations generally had higher survival and obtained a greater maximum size than foreign individuals, regardless of warming treatment. Phenological traits varied with latitude of the source population, such that southern populations demonstrated substantially delayed leaf‐out and senescence relative to northern populations. Our results suggest that environmental conditions other than temperature may influence the ability of foreign populations and species to establish at more northerly latitudes as the climate warms, potentially leading to lags in northward range shifts for some species.     

Responses of coral reef fishes to past climate changes are related to life‐history traits

Coral reefs and their associated fauna are largely impacted by ongoing climate change. Unravelling species responses to past climatic variations might provide clues on the consequence of ongoing changes. Here, we tested the relationship between changes in sea surface temperature and sea levels during the Quaternary and present‐day distributions of coral reef fish species. We investigated whether species‐specific responses are associated with life‐history traits. We collected a database of coral reef fish distribution together with life‐history traits for the Indo‐Pacific Ocean. We ran species distribution models (SDMs) on 3,725 tropical reef fish species using contemporary environmental factors together with a variable describing isolation from stable coral reef areas during the Quaternary. We quantified the variance explained independently by isolation from stable areas in the SDMs and related it to a set of species traits including body size and mobility. The variance purely explained by isolation from stable coral reef areas on the distribution of extant coral reef fish species largely varied across species. We observed a triangular relationship between the contribution of isolation from stable areas in the SDMs and body size. Species, whose distribution is more associated with historical changes, occurred predominantly in the Indo‐Australian archipelago, where the mean size of fish assemblages is the lowest. Our results suggest that the legacy of habitat changes of the Quaternary is still detectable in the extant distribution of many fish species, especially those with small body size and the most sedentary. Because they were the least able to colonize distant habitats in the past, fish species with smaller body size might have the most pronounced lags in tracking ongoing climate change.     

Incorporating local adaptation into forecasts of species’ distribution and abundance under climate change

Populations of many species are genetically adapted to local historical climate conditions. Yet most forecasts of species’ distributions under climate change have ignored local adaptation (LA), which may paint a false picture of how species will respond across their geographic ranges. We review recent studies that have incorporated intraspecific variation, a potential proxy for LA, into distribution forecasts, assess their strengths and weaknesses, and make recommendations for how to improve forecasts in the face of LA. The three methods used so far (species distribution models, response functions, and mechanistic models) reflect a trade‐off between data availability and the ability to rigorously demonstrate LA to climate. We identify key considerations for incorporating LA into distribution forecasts that are currently missing from many published studies, including testing the spatial scale and pattern of LA, the confounding effects of LA to nonclimatic or biotic drivers, and the need to incorporate empirically based dispersal or gene flow processes. We suggest approaches to better evaluate these aspects of LA and their effects on species‐level forecasts. In particular, we highlight demographic and dynamic evolutionary models as promising approaches to better integrate LA into forecasts, and emphasize the importance of independent model validation. Finally, we urge closer examination of how LA will alter the responses of central vs. marginal populations to allow stronger generalizations about changes in distribution and abundance in the face of LA.     

Characterizing the contribution of plasticity and genetic differentiation to community‐level trait responses to environmental change

The match between functional trait variation in communities and environmental gradients is maintained by three processes: phenotypic plasticity and genetic differentiation (intraspecific processes), and species turnover (interspecific). Recently, evidence has emerged suggesting that intraspecific variation might have a potentially large role in driving functional community composition and response to environmental change. However, empirical evidence quantifying the respective importance of phenotypic plasticity and genetic differentiation relative to species turnover is still lacking. We performed a reciprocal transplant experiment using a common herbaceous plant species (Oxalis montana) among low‐, mid‐, and high‐elevation sites to first quantify the contributions of plasticity and genetic differentiation in driving intraspecific variation in three traits: height, specific leaf area, and leaf area. We next compared the contributions of these intraspecific drivers of community trait–environment matching to that of species turnover, which had been previously assessed along the same elevational gradient. Plasticity was the dominant driver of intraspecific trait variation across elevation in all traits, with only a small contribution of genetic differentiation among populations. Local adaptation was not detected to a major extent along the gradient. Fitness components were greatest in O. montana plants with trait values closest to the local community‐weighted means, thus supporting the common assumption that community‐weighted mean trait values represent selective optima. Our results suggest that community‐level trait responses to ongoing climate change should be mostly mediated by species turnover, even at the small spatial scale of our study, with an especially small contribution of evolutionary adaptation within species.     

How plant life‐history and ecological traits relate to species rarity and commonness at varying spatial scales

Comparative studies investigating relationships between plant traits and species rarity and commonness were surveyed to establish whether global patterns have emerged that would be of practical use in management strategies aimed at the long‐term conservation of species. Across 54 studies, 94 traits have been examined in relation to abundance, distribution and threatened status at local, regional and geographical spatial scales. Most traits (63) have yet to be the focus of more than one study. Half of the studies involved less than 10 species, and one‐quarter did not replicate rare–common contrasts. Although these features of the literature make it difficult to demonstrate robust generalizations regarding trait relationships with species rarity, some important findings surfaced in relation to traits that have been examined in two or more studies. Species with narrow geographical distributions were found to produce significantly fewer seeds (per unit measurement) than common species (in four of six studies), but did not differ with respect to breeding system (five of five studies). The majority of traits (including seed size, competitive ability, growth form and dispersal mode) were related to rarity in different ways from one study to the next. The highly context‐dependent nature of most trait relationships with rarity implies that application of knowledge concerning rare–common differences and similarities to management plans will vary substantially for different vegetation types and on different continents. A comparative analysis of distribution patterns in relation to several life‐history and ecological traits among 700 Australian eucalypt species was then performed. A significantly dispro­portionate number of tall species and species with long flowering durations had wide geographical ranges. Trait relationships with distribution were explored further through the development of a methodology incorporating multiple spatial scales. Eight theoretical categories were described illustrating variation in distribution patterns (and hence rarity and commonness) across small, intermediate and large spatial scales, based on the spatial structure of species occurrence across the Australian landscape. Each eucalypt species was placed into a category, and trait variation was explored across all species in relation to distribution patterns across multiple spatial scales. This approach yielded important information about trait relationships with distribution among the eucalypts, linking the spatial structure of points‐of‐occurrence with patterns of rarity and commonness. With the pressing need to protect increasing numbers of threatened species and slow rates of extinction, the development and refinement of a broadly usable methodology for rarity studies that encompasses multiple spatial scales, which can be used for any geographical location, will be useful in both conservation and management.     

Ecophysiological constraints shape autumn migratory response to climate change in the North American field sparrow

Our ability to accurately forecast species' geographical responses to climate change requires knowledge of the proximate and ultimate drivers of their distribution. Here, we consider the ecophysiological and demographic determinants of the distribution of a partial migrant, the North American field sparrow, Spizella pusilla. From 1940 to 1963, the field sparrow extended its winter northern range margin 222km polewards. Such expansion was coincident with not only a geographical expansion into suitable breeding habitats, but also a decrease in mean abundance across sites occupied during the winter surveys. Combined, these trends suggest that declining populations along the expansion front either stopped migrating or altered their autumn migration. The poleward expansion was not coincident with climatically induced decreases in peak metabolic energy demand, but it did track increases in ecosystem net primary productivity. After 1963, the species' lower lethal temperature prevented further poleward movement. These findings show how different ecophysiological constraints can interact to change migration and distribution in a demographically declining species.     

Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Differences in population vulnerability to warming are defined by spatial patterns in thermal adaptation. These patterns may be driven by natural selection over spatial environmental gradients, but can also be shaped by gene flow, especially in marine taxa with high dispersal potential. Understanding and predicting organismal responses to warming requires disentangling the opposing effects of selection and gene flow. We begin by documenting genetic divergence of thermal tolerance and developmental phenotypic plasticity. Ten populations of the widespread copepod Acartia tonsa were collected from sites across a large thermal gradient, ranging from the Florida Keys to Northern New Brunswick, Canada (spanning over 20° latitude). Thermal performance curves (TPCs) from common garden experiments revealed local adaptation at the sampling range extremes, with thermal tolerance increasing at low latitudes and decreasing at high latitudes. The opposite pattern was observed in phenotypic plasticity, which was strongest at high latitudes. No relationship was observed between phenotypic plasticity and environmental variables. Instead, the results are consistent with the hypothesis of a trade‐off between thermal tolerance and the strength of phenotypic plasticity. Over a large portion of the sampled range, however, we observed a remarkable lack of differentiation of TPCs. To examine whether this lack of divergence is the result of selection for a generalist performance curve or constraint by gene flow, we analyzed cytochrome oxidase I mtDNA sequences, which revealed four distinct genetic clades, abundant genetic diversity, and widely distributed haplotypes. Strong divergence in thermal performance within genetic clades, however, suggests that the pace of thermal adaptation can be relatively rapid. The combined insight from the laboratory physiological experiments and genetic data indicate that gene flow constrains differentiation of TPCs. This balance between gene flow and selection has implications for patterns of vulnerability to warming. Taking both genetic differentiation and phenotypic plasticity into account, our results suggest that local adaptation does not increase vulnerability to warming, and that low‐latitude populations in general may be more vulnerable to predicted temperature change over the next century.     

Stable and variable life‐history responses to temperature and photoperiod in the beet webworm,Loxostege sticticalis

The beet webworm, Loxostege sticticalis L. (Lepidoptera: Crambidae), unlike many temperate insects and despite its wide distribution range, has a geographically stable value of the critical photoperiod for diapause induction. It has thus been hypothesized that the species could adjust its life cycle to different climates in an alternative way, which should be reflected in geographical variation and/or environmental plasticity of some other ecophysiological trait. Three remote populations of the beet webworm were studied. The insects were reared from egg to adult at several combinations of temperature and photoperiod in order to measure development times of all the immature stages and pre‐pupal body weight, and to characterize the sensitivity of these life‐history traits to the two ecological factors. The thermal reaction norms for immature development appeared to be significantly different in the three populations. There was also a significant effect of photoperiod on development time as well as on the thermal sensitivity and lower temperature threshold for larval development. Pre‐pupae from the northernmost population were heavier and their body mass was more strongly affected by photoperiod than in the other two, but attainment of a greater weight under short‐day conditions, especially combined with higher temperatures, was common for all the three populations. Nevertheless, all the discovered geographical and environmentally induced differences in life‐history traits were very small and their adaptive significance remains problematic.