Variation in plant thermal reaction norms along a latitudinal gradient – more than adaptation to season length

Little is known about the extent to which observed phenological responses to changes in climate are the result of phenotypic plasticity or genetic changes. We also know little about how plasticity, in terms of thermal reaction norms, vary spatially. We investigated if the thermal reaction norms for flower development of five crucifer species (Brassicaceae) differed among three regions along a south–north latitudinal gradient in replicated experiments. The mean response (elevation) of thermal reaction norms of flowering differed among regions in all study species, while sensitivity of flower development to temperature (slope) differed in only one of the species. Differences in mean responses corresponded to cogradient patterns in some species, but countergradient patterns in other. This suggests that differences among regions were not solely the result of adaptation to differences in the length of the growing season, but that other factors, such as herbivory, play an important role. Differences in development rate within species were mainly explained by variation in early phases of bud formation in some species but by variation in later phases of bud formation in other species. The differences in latitudinal patterns of thermal reaction norms among species observed in this study are important, both to identify agents of selection and to predict short‐ and long‐term responses to a warming climate.     

Local divergence of thermal reaction norms among amphibian populations is affected by pond temperature variation

Although temperature variation is known to cause large‐scale adaptive divergence, its potential role as a selective factor over microgeographic scales is less well‐understood. Here, we investigated how variation in breeding pond temperature affects divergence in multiple physiological (thermal performance curve and critical thermal maximum [CT_max]) and life‐history (thermal developmental reaction norms) traits in a network of Rana arvalis populations. The results supported adaptive responses to face two main constraints limiting the evolution of thermal adaptation. First, we found support for the faster–slower model, indicating an adaptive response to compensate for the thermodynamic constraint of low temperatures in colder environments. Second, we found evidence for the generalist–specialist trade‐off with populations from colder and less thermally variable environments exhibiting a specialist phenotype performing at higher rates but over a narrower range of temperatures. By contrast, the local optimal temperature for locomotor performance and CT_max did not match either mean or maximum pond temperatures. These results highlight the complexity of the adaptive multiple‐trait thermal responses in natural populations, and the role of local thermal variation as a selective force driving diversity in life‐history and physiological traits in the presence of gene flow.     

Divergence and ontogenetic coupling of larval behaviour and thermal reaction norms in three closely related butterflies

Genetic trade-offs such as between generalist–specialist strategies can be masked by changes in compensatory processes involving energy allocation and acquisition which regulation depends on the state of the individual and its ecological surroundings. Failure to account for such state dependence may thus lead to misconceptions about the trade-off structure and nature of constraints governing reaction norm evolution. Using three closely related butterflies, we first show that foraging behaviours differ between species and change remarkably throughout ontogeny causing corresponding differences in the thermal niches experienced by the foraging larvae. We further predicted that thermal reaction norms for larval growth rate would show state-dependent variation throughout development as a result of selection for optimizing feeding strategies in the respective foraging niches of young and old larvae. We found substantial developmental plasticity in reaction norms that was species-specific and reflected the different ontogenetic niche shifts. Any conclusions regarding constraints on performance curves or species-differentiation in thermal physiology depend on when reaction norms were measured. This demonstrates that standardized estimates at single points in development, or in general, allow variation in only one ecological dimension, may sometimes provide incomplete information on reaction norm constraints.     

Temperature adaptation in a geographically widespread zooplankter,Daphnia magna

Evidence for temperature adaptation in Daphnia magna was inferred from variation in the shape of temperature reaction norms for somatic growth rate, a fitness‐related trait. Ex‐ephippial clones from eight populations across Europe were grown under standardized conditions after preacclimation at five temperatures (17–29 °C). Significant variation for grand mean growth rates occurred both within populations (among clones) and between populations. Genetic variation for reaction norm shape was found within populations, with temperature‐dependent trade‐offs in clone relative fitness. However, the population average responses to temperature were similar, following approximately parallel reaction norms. The among‐population variation is not evidence for temperature adaptation. Lack of temperature adaptation at the population level may be a feature of intermittent populations where environmentally terminated diapause can entrain the planktonic stage of the life‐history within a similar range of temperatures.     

Thermal reaction norms in two Coenagrion damselfly species: contrasting embryonic and larval life-history traits

1. We studied the temperature‐dependence of important life‐history traits both at the embryonic (egg hatching success, embryonic development time and hatchling size) and the larval stage (larval growth rate, larval survival and larval size after 100 days) using full‐sib families of two congeneric damselflies, Coenagrion hastulatum and Coenagrion puella, that differ in latitudinal distribution. Larvae were reared in the laboratory from the egg stage at four temperatures (12, 17, 22 and 27 °C). 2. The observed patterns of thermal plasticity in embryonic traits showed that the northern species was more successful than the southern species at lower temperatures, in line with the pattern of temperature adaptation in thermal reaction norms. 3. At the larval stage, we found no consistent pattern of latitudinal compensation. The thermal family reaction norms indicate, however, the potential for latitudinal compensation to evolve. We observed an ontogenetic shift in thermal optima for larval growth rate, with a higher optimal temperature for growth rate during the first 2 weeks of the larval stage. 4. This is the first indication of the existence of latitudinal compensation at the interspecific level in an invertebrate; it is stage‐specific, being present only in the embryonic stage. We argue that compensation in the embryonic stage may be much more likely than in the larvae and stress the importance of including more then one life‐history stage when drawing conclusions about the adaptiveness of patterns in thermal reaction norms.     

Latitudinal and voltinism compensation shape thermal reaction norms for growth rate

Latitudinal variation in thermal reaction norms of key fitness traits may inform about the response of populations to climate warming, yet their adaptive nature and evolutionary potential are poorly known. We assessed the contribution of quantitative genetic, neutral genetic and environmental effects to thermal reaction norms of growth rate for populations of the damselfly Ischnura elegans. Among populations, reaction norms differed primarily in elevation, suggesting that time constraints associated with shorter growth seasons in univoltine, high-latitude as well as multivoltine, low-latitude populations selected for faster growth rates. Phenotypic divergence among populations is consistent with selection rather than drift as Q(ST) was greater than F(ST) in all cases. Q(ST) estimates increased with experimental temperature and were influenced by genotype by environment interactions. Substantial additive genetic variation for growth rate in all populations suggests that evolution of trait means in different environments is not constrained. Heritability of growth rates was higher at high temperature, driven by increased genetic rather than environmental variance. While environment-specific nonadditive effects also may contribute to heritability differences among temperatures, maternal effects did not play a significant role (where these could be accounted for). Genotype by environment interactions strongly influenced the adaptive potential of populations, and our results suggest the potential for microevolution of thermal reaction norms in each of the studied populations. In summary, the observed latitudinal pattern in growth rates is adaptive and results from a combination of latitudinal and voltinism compensation. Combined with the evolutionary potential of thermal reaction norms, this may affect populations' ability to respond to future climate warming.     

Keeping your options open: Maintenance of thermal plasticity during adaptation to a stable environment

Phenotypic plasticity may allow species to cope with environmental variation. The study of thermal plasticity and its evolution helps understanding how populations respond to variation in temperature. In the context of climate change, it is essential to realize the impact of historical differences in the ability of populations to exhibit a plastic response to thermal variation and how it evolves during colonization of new environments. We have analyzed the real‐time evolution of thermal reaction norms of adult and juvenile traits in Drosophila subobscura populations from three locations of Europe in the laboratory. These populations were kept at a constant temperature of 18ºC, and were periodically assayed at three experimental temperatures (13ºC, 18ºC, and 23ºC). We found initial differentiation between populations in thermal plasticity as well as evolutionary convergence in the shape of reaction norms for some adult traits, but not for any of the juvenile traits. Contrary to theoretical expectations, an overall better performance of high latitude populations across temperatures in early generations was observed. Our study shows that the evolution of thermal plasticity is trait specific, and that a new stable environment did not limit the ability of populations to cope with environmental challenges.     

Inter- and intrapopulation variation in thermal reaction norms for growth rate: evolution of latitudinal compensation in ectotherms with a genetic constraint

In ectotherms, lower temperatures in high-latitude environments would theoretically reduce the annual growth rates of individuals. If slower growth and resultant smaller body size reduce fitness, individuals in higher latitudes may evolve compensatory responses. Two alternative models of such latitudinal compensation are possible: Model I: thermal reaction norms for growth rates of high-latitude individuals may be horizontally shifted to a lower range of temperatures, or Model II: reaction norms may be vertically shifted so that high-latitude individuals can grow faster across all temperatures. Model I is expected when annual growth rates in the wild are only a function of environmental temperatures, whereas Model II is expected when individuals in higher latitudes can only grow during a shorter period of a year. A variety of mixed strategies of these two models are also possible, and the magnitude of horizontal versus vertical variation in reaction norms among latitudinal populations will be indicative of the importance of "temperature" versus "seasonality" in the evolution of latitudinal compensation. However, the form of latitudinal compensation may be affected by possible genetic constraints due to the genetic architecture of reaction norms. In this study, we examine the inter- and intrapopulation variations in thermal reaction norms for growth rate of the medaka fish Oryzias latipes. Common-environment experiments revealed that average reaction norms differed primarily in elevation among latitudinal populations in a manner consistent with Model II (adaptation to "seasonality"), suggesting that natural selection in high latitudes prefers individuals that grow faster even within a shorter growing season to individuals that have longer growing seasons by growing at lower temperatures. However, intrapopulation variation in reaction norms was also vertical: some full-sibling families grew faster than others across all temperatures examined. This tendency in intrapopulation genetic variation for thermal reaction norms may have restricted the evolution of latitudinal compensation, irrespective of the underlying selection pressure.     

Thermal plasticity of growth and development varies adaptively among alternative developmental pathways

Polyphenism, the expression of discrete alternative phenotypes, is often a consequence of a developmental switch. Physiological changes induced by a developmental switch potentially affect reaction norms, but the evolution and existence of alternative reaction norms remains poorly understood. Here, we demonstrate that, in the butterfly Pieris napi (Lepidoptera: Pieridae), thermal reaction norms of several life history traits vary adaptively among switch‐induced alternative developmental pathways of diapause and direct development. The switch was affected both by photoperiod and temperature, ambient temperature during late development having the potential to override earlier photoperiodic cues. Directly developing larvae had higher development and growth rates than diapausing ones across the studied thermal gradient. Reaction norm shapes also differed between the alternative developmental pathways, indicating pathway‐specific selection on thermal sensitivity. Relative mass increments decreased linearly with increasing temperature and were higher under direct development than diapause. Contrary to predictions, population phenology did not explain trait variation or thermal sensitivity, but our experimental design probably lacks power for finding subtle phenology effects. We demonstrate adaptive differentiation in thermal reaction norms among alternative phenotypes, and suggest that the consequences of an environmentally dependent developmental switch primarily drive the evolution of alternative thermal reaction norms in P. napi.     

SEASONALLY VARYING DIET QUALITY AND THE QUANTITATIVE GENETICS OF DEVELOPMENT TIME AND BODY SIZE IN BIRCH FEEDING INSECTS

Abstract Genetic variance‐covariance structures (G), describing genetic constraints on microevolutionary changes of populations, have a central role in the current theories of life‐history evolution. However, the evolution of Gs in natural environments has been poorly documented. Resource quality and quantity for many animals and plants vary seasonally, which may shape genetic architectures of their life histories. In the mountain birch‐insect herbivore community, leaf quality of birch for insect herbivores declines profoundly during both leaf growth and senescence, but remains stable during midsummer. Using six sawfly species specialized on the mountain birch foliage, we tested the ways in which the seasonal variation in foliage quality of birch is related to the genetic architectures of larval development time and body size. In the species consuming mature birch leaves of stable quality, that is, without diet‐imposed time constraints for development time, long development led to high body mass. This was revealed by the strongly positive phenotypic and genetic correlations between the traits. In the species consuming growing or senescing leaves, on the other hand, the rapidly deteriorating leaf quality prevented the larvae from gaining high body mass after long development. In these species, the phenotypic and genetic correlations between development time and final mass were negative or zero. In the early‐summer species with strong selection for rapid development, genetic variation in development time was low. These results show that the intuitively obvious positive genetic relationship between development time and final body mass is a probable outcome only when the constraints for long development are relaxed. Our study provides the first example of a modification in guild‐wide patterns in the genetic architectures brought about by seasonal variation in resource quality.     

THE EVOLUTION OF ENVIRONMENTAL TOLERANCE AND RANGE SIZE: A COMPARISON OF GEOGRAPHICALLY RESTRICTED AND WIDESPREAD MIMULUS

The geographic ranges of closely related species can vary dramatically, yet we do not fully grasp the mechanisms underlying such variation. The niche breadth hypothesis posits that species that have evolved broad environmental tolerances can achieve larger geographic ranges than species with narrow environmental tolerances. In turn, plasticity and genetic variation in ecologically important traits and adaptation to environmentally variable areas can facilitate the evolution of broad environmental tolerance. We used five pairs of western North American monkeyflowers to experimentally test these ideas by quantifying performance across eight temperature regimes. In four species pairs, species with broader thermal tolerances had larger geographic ranges, supporting the niche breadth hypothesis. As predicted, species with broader thermal tolerances also had more within‐population genetic variation in thermal reaction norms and experienced greater thermal variation across their geographic ranges than species with narrow thermal tolerances. Species with narrow thermal tolerance may be particularly vulnerable to changing climatic conditions due to lack of plasticity and insufficient genetic variation to respond to novel selection pressures. Conversely, species experiencing high variation in temperature across their ranges may be buffered against extinction due to climatic changes because they have evolved tolerance to a broad range of temperatures.     

An empirical test for a zone of canalization in thermal reaction norms

Theoretical models on the evolution of phenotypic plasticity predict a zone of canalization where reaction norms cross, and genetic variation is minimized in the environment a population most frequently encounter. Empirical tests of this prediction are largely missing, in particular for life‐history traits. We addressed this prediction by quantifying thermal reaction norms of three life‐history traits (somatic growth rate, age and size at maturation) of a Norwegian population of Daphnia magna and testing for the occurrence of an intermediate temperature (T_m) at which genetic variance in the traits is minimized. Size at maturation changed relatively little with temperature compared to the other traits, and there was no genetic variance in the shape of the reaction norm. Consequently, age at maturation and somatic growth rate were strongly negatively correlated. Both traits showed a strong genotype–environment interaction, and the estimated T_m was 14 °C for both age at maturation and growth rate. This value of T_m corresponds well with mean summer temperatures experienced by the population and suggests that the population has evolved under stabilizing selection in temperatures that fluctuate around this mean temperature. These results suggest local adaptation to temperature in the studied population and allow predicting evolutionary trajectories of thermal reaction norms under changing thermal regimes.     

Phenotypic constraints and community structure: Linking trade‐offs within and among species

Trade‐offs are central to many topics in biology, from the evolution of life histories to ecological mechanisms of species coexistence. Trade‐offs observed among species may reflect pervasive constraints on phenotypes that are achievable given biophysical and resource limitations. If so, then among‐species trade‐offs should be consistent with trade‐offs within species. Alternatively, trait variation among co‐occurring species may reflect historical contingencies during community assembly rather than within‐species constraints. Here, we test whether a key trade‐off between relative growth rate (RGR) and water‐use efficiency (WUE) among Sonoran Desert winter annual plants is apparent within four species representing different strategies in the system. We grew progeny of maternal families from multiple populations in a greenhouse common garden. One species, Pectocarya recurvata, displayed the expected RGR–WUE trade‐off among families within populations. For other species, although RGR and WUE often varied clinally among populations, among‐family variation within populations was lacking, implicating a role for past selection on these traits. Our results suggest that a combination of limited genetic variation in single traits and negative trait correlations could pose constraints on the evolution of a high‐RGR and high‐WUE phenotype within species, providing a microevolutionary explanation for phenotypes that influence community‐level patterns of abundance and coexistence.     

Selection on an extreme weapon in the frog‐legged leaf beetle (Sagra femorata)

Biologists have been fascinated with the extreme products of sexual selection for decades. However, relatively few studies have characterized patterns of selection acting on ornaments and weapons in the wild. Here, we measure selection on a wild population of weapon‐bearing beetles (frog‐legged leaf beetles: Sagra femorata) for two consecutive breeding seasons. We consider variation in both weapon size (hind leg length) and in relative weapon size (deviations from the population average scaling relationship between hind leg length and body size), and provide evidence for directional selection on weapon size per se and stabilizing selection on a particular scaling relationship in this population. We suggest that whenever growth in body size is sensitive to external circumstance such as nutrition, then considering deviations from population‐level scaling relationships will better reflect patterns of selection relevant to evolution of the ornament or weapon than will variation in trait size per se. This is because trait‐size versus body‐size scaling relationships approximate underlying developmental reaction norms relating trait growth with body condition in these species. Heightened condition‐sensitive expression is a hallmark of the exaggerated ornaments and weapons favored by sexual selection, yet this plasticity is rarely reflected in the way we think about—and measure—selection acting on these structures in the wild.     

Temperature-dependent plasticity of segment number in an arthropod species: the centipede Strigamia maritima

SUMMARY The evolution of arthropod segment number provides us with a paradox, because, whereas there is more than 20‐fold variation in this character overall, most classes and orders of arthropods are composed of species that lack any variation in the number of segments. So, what is the origin of the higher‐level variation? The centipede order Geophilomorpha is unusual because, with the exception of one of its families, all species exhibit intraspecific variation in segment number. Hence it provides an opportunity to investigate how segment number may change in a microevolutionary context. Here, we show that segment number can be directly altered by an environmental factor (temperature)—this is the first such demonstration for any arthropod. The direction of the effect is such that higher temperature during embryogenesis produces more segments. This potentially explains an intraspecific cline in the species concerned, Strigamia maritima, but it does not explain how such a cline is translated into the parallel interspecific pattern of lower‐latitude species having more segments. Given the plastic nature of the intraspecific variation, its link with interspecific differences may lie in selection acting on developmental reaction norms.     

Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle

The majority of ectotherms grow slower but mature at a larger body size in colder environments. This phenomenon has puzzled biologists because classic theories of life-history evolution predict smaller sizes at maturity in environments that retard growth. During the last decade, intensive theoretical and empirical research has generated some plausible explanations based on nonadaptive or adaptive plasticity. Nonadaptive plasticity of body size is hypothesized to result from thermal constraints on cellular growth that cause smaller cells at higher temperatures, but the generality of this theory is poorly supported. Adaptive plasticity is hypothesized to result from greater benefits or lesser costs of delayed maturation in colder environments. These theories seem to apply well to some species but not others. Thus, no single theory has been able to explain the generality of temperature-size relationships in ectotherms. We recommend a multivariate theory that focuses on the coevolution of thermal reaction norms for growth rate and size at maturity. Such a theory should incorporate functional constraints on thermal reaction norms, as well as the natural covariation between temperature and other environmental variables.     

Searching for constraints by cross‐species comparison: reaction norms for age and size at maturity in insects

An evolutionary explanation should consider the balance between environmentally‐based selective pressures, and the resistance of the organism's phenotype to adaptive evolution, with the latter being captured by the concept of constraint. The limited attention to non‐adaptive explanations in evolutionary ecology is at least partly caused by methodological difficulties with respect to identifying and quantifying constraints. As an example of an experimental approach evaluating a constraint‐based explanation, we present a cross‐species comparison of the shape of reaction norms for size and age at maturity. Instar‐ and sex‐specific development times and final sizes were recorded for two distantly‐related species of insects (Lepidoptera), with larval growth rates being manipulated by means of refined starvation treatments. We found that (1) the ‘classical’ L‐shaped reaction norms for final size and development time are characteristic also of individual larval instars; (2) these responses show a high degree of quantitative similarity across the species, different larval instars, and sexes within species; and (3) the similarity among species and sexes is higher for the penultimate than for the final instar. The high degree of similarity suggests that some physiological mechanisms determining such reaction norms are evolutionarily conservative. An alternative explanation (i.e. quantitative similarity of ecologically based selective pressures) appears less likely. The results of a previous study on a third lepidopteran species not only support our general conclusions, but also provide a clear case of adaptive evolution in some aspects of such reaction norms. The present study shows one way how the data required to measure evolutionary conservatism in reaction norms for body size can be obtained empirically. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 296–307.     

Experimental evolution for generalists and specialists reveals multivariate genetic constraints on thermal reaction norms

Theory predicts the emergence of generalists in variable environments and antagonistic pleiotropy to favour specialists in constant environments, but empirical data seldom support such generalist–specialist trade‐offs. We selected for generalists and specialists in the dung fly Sepsis punctum (Diptera: Sepsidae) under conditions that we predicted would reveal antagonistic pleiotropy and multivariate trade‐offs underlying thermal reaction norms for juvenile development. We performed replicated laboratory evolution using four treatments: adaptation at a hot (31 °C) or a cold (15 °C) temperature, or under regimes fluctuating between these temperatures, either within or between generations. After 20 generations, we assessed parental effects and genetic responses of thermal reaction norms for three correlated life‐history traits: size at maturity, juvenile growth rate and juvenile survival. We find evidence for antagonistic pleiotropy for performance at hot and cold temperatures, and a temperature‐mediated trade‐off between juvenile survival and size at maturity, suggesting that trade‐offs associated with environmental tolerance can arise via intensified evolutionary compromises between genetically correlated traits. However, despite this antagonistic pleiotropy, we found no support for the evolution of increased thermal tolerance breadth at the expense of reduced maximal performance, suggesting low genetic variance in the generalist–specialist dimension.     

Differences in leaf thermoregulation and water use strategies between three co‐occurring Atlantic forest tree species

Given anticipated climate changes, it is crucial to understand controls on leaf temperatures including variation between species in diverse ecosystems. In the first study of leaf energy balance in tropical montane forests, we observed current leaf temperature patterns on 3 tree species in the Atlantic forest, Brazil, over a 10‐day period and assessed whether and why patterns may vary among species. We found large leaf‐to‐air temperature differences (maximum 18.3 °C) and high leaf temperatures (over 35 °C) despite much lower air temperatures (maximum 22 °C). Leaf‐to‐air temperature differences were influenced strongly by radiation, whereas leaf temperatures were also influenced by air temperature. Leaf energy balance modelling informed by our measurements showed that observed differences in leaf temperature between 2 species were due to variation in leaf width and stomatal conductance. The results suggest a trade‐off between water use and leaf thermoregulation; Miconia cabussu has more conservative water use compared with Alchornea triplinervia due to lower transpiration under high vapour pressure deficit, with the consequence of higher leaf temperatures under thermal stress conditions. We highlight the importance of leaf functional traits for leaf thermoregulation and also note that the high radiation levels that occur in montane forests may exacerbate the threat from increasing air temperatures.