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.     

The physiological basis of reaction norms: the interaction among growth rate, the duration of growth and body size

The general effects of temperature and nutritional quality ongrowth rate and body size are well known. We know little, however,about the physiological mechanisms by which an organism translatesvariation in diet and temperature into reaction norms of bodysize or development time. We outline an endocrine-based physiologicalmechanism that helps explain how this translation occurs inthe holometabolous insect Manduca sexta (Sphingidae). Body sizeand development time are controlled by three factors: (i) growthrate, (ii) the timing of the cessation of juvenile hormone secretion(measured by the critical weight) and (iii) the timing of ecdysteroidsecretion leading to pupation (the interval to cessation ofgrowth [ICG] after reaching the critical weight). Thermal reactionnorms of body size and development time are a function of howthese three factors interact with temperature. Body size issmaller at higher temperatures, because the higher growth ratedecreases the ICG, thereby reducing the amount of mass thatcan accumulate. Development time is shorter at higher temperaturesbecause the higher growth rate decreases the time required toattain the critical weight and, independently, controls theduration of the ICG. Life history evolution along altitudinal,latitudinal and seasonal gradients may occur through differentialselection on growth rate and the duration of the two independentlycontrolled determinants of the growth period.     

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.     

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.     

Temperature-induced gene expression associated with different thermal reaction norms for growth rate

Although nearly all organisms are subject to fluctuating temperature regimes in their natural habitat, little is known about the genetics underlying the response to thermal conditions, and even less about the genetic differences that cause individual variation in thermal response. Here, we aim to elucidate possible pathways involved in temperature-induced phenotypic plasticity of growth rate. Our model organism is the collembolan Orchesella cincta that occurs in a wide variety of habitats and is known to be adapted to local thermal conditions. Because sequence information is lacking in O. cincta, we constructed cDNA libraries enriched for temperature-responsive genes using suppression subtractive hybridization. We compared gene expression of O. cincta with steep thermal reaction norms (high plasticity) to those with flat thermal reaction norms (low plasticity) for juvenile growth after exposure to a temperature switch composed of a cooling or a warming treatment. Using suppression subtractive hybridization, we found differential expression of ten nuclear genes, including several genes involved in energy metabolism, such as pantothenate kinase and carbonic anhydrase. In addition, seven mitochondrial genes were found in the cloned subtracted library, but further analysis showed this was caused by allelic variation in mitochondrial genes in our founder population, and that a specific haplotype was associated with high thermal responsiveness. Future work will focus on candidate genes from pathways such as the oxidative phosphorylation and biosynthesis of coenzyme A which are possibly involved in thermal responsiveness of juvenile growth rate.     

Plasticity of size and growth in fluctuating thermal environments: comparing reaction norms and performance curves

Ectothermic animals exhibit two distinct kinds of plasticityin response to temperature: Thermal performance curves (TPCs),in which an individual's performance (e.g., growth rate) variesin response to current temperature; and developmental reactionnorms (DRNs), in which the trait value (e.g., adult body sizeor development time) of a genotype varies in response to developmentaltemperatures experienced over some time period during development.Here we explore patterns of genetic variation and selectionon TPCs and DRNs for insects in fluctuating thermal environments.First, we describe two statistical methods for partitioningtotal genetic variation into variation for overall size or performanceand variation in plasticity, and apply these methods to availabledatasets on DRNs and TPCs for insect growth and size. Our resultsindicate that for the datasets we considered, genetic variationin plasticity represents a larger proportion of the total geneticvariation in TPCs compared to DRNs, for the available datasets.Simulations suggest that estimates of the genetic variationin plasticity are strongly affected by the number and rangeof temperatures considered, and by the degree of nonlinearityin the TPC or DRN. Second, we review a recent analysis of fieldselection studies which indicates that directional selectionfavoring increased overall size is common in many systems—thatbigger is frequently fitter. Third, we use a recent theoreticalmodel to examine how selection on thermal performance curvesrelates to environmental temperatures during selection. Themodel predicts that if selection acts primarily on adult sizeor development time, then selection on thermal performance curvesfor larval growth or development rates is directly related tothe frequency distribution of temperatures experienced duringlarval development. Using data on caterpillar temperatures inthe field, we show that the strength of directional selectionon growth rate is predicted to be greater at the modal (mostfrequent) temperatures, not at the mean temperature or at temperaturesat which growth rate is maximized. Our results illustrate someof the differences in genetic architecture and patterns of selectionbetween thermal performance curves and developmental reactionnorms.     

The evolution of prey body size reaction norms in diverse communities

1. Heterogeneous predation risks can select for predator-specific plastic defences in prey populations. However, diverse predation threats can generate diffuse selection, which, in turn, can lead to the evolution of more generalized reaction norms. Unreliable predator cues also can select for more generalized plasticity in prey. 2. Here, I evaluated the extent to which variation in risk from a focal predator vs. variation in risk from predator diversity and composition were associated with variation in body mass reaction norms in 18 prey populations. Toward this end, I assayed the body mass reaction norms in a common garden experiment for spotted salamander larvae Ambystoma maculatum in response to marbled salamander predators Ambystoma opacum, local predator richness and the densities of two auxiliary predator species. 3. When raised under controlled conditions, prey larvae generally were smaller when exposed to A. opacum kairomones. Among populations, the mean and slope of body mass variation was unrelated to A. opacum's local density. 4. Predator richness and several key environmental factors were not associated with reaction norm variation. Instead, the density of an auxiliary newt predator species was correlated with reduced mass reaction norm slopes. Results suggest that diffuse selection from auxiliary predators can modify the evolution of life-history plasticity.     

Evolution of body size: an optimization model

The growth of individuals is often described by bioenergetic equations which partition assimilated energy into maintenance, growth, reproduction, and so on. Such energy flows vary with body size. The bioenergetic equations in this paper, under the assumptions that organisms will adopt behavior that channels a maximum amount of energy into the production of surviving progeny, produce a model optimizing growth and reproduction. Using the Weierstrass theorem, we show that a solution of the optimization problem exists. The problem is further solved analytically using the Pontryagin maximum principle. The main conclusion of the paper is that in a given environment an optimal body size exists, one which maximizes the energy channeled to the production of progeny. This body size depends on the mortality rate, the maximum life span, and the derivative of the growth equation with respect to body size. The biological results predicted from the model are compared with ecological data for zooplankton and vertebrate species, which support the conclusions obtained.     

The analysis of reaction norms for age and size at maturity using maturation rate models

Reaction norms for age and size at maturity are being analyzed to answer important questions about the evolution of life histories. A new statistical method is developed in the framework of time-to-event data analysis, which circumvents shortcomings in currently available approaches. The method emphasizes the estimation of age- and size-dependent maturation rates. Individual probabilities of maturation during any given time interval follow by integrating maturation rate along the growth curve. The integration may be performed in different ways, over ages or sizes or both, corresponding to different assumptions on how individuals store the operational history of the maturation process. Data analysis amounts to fitting generalized nonlinear regression models to a maturation status variable. This technique has three main advantages over existing methods: (1) treating maturation as a stochastic process enables one to specify a rate of maturation; (2) age and size at which maturation occurs do not have to be observed exactly, and bias arising from approximations and interpolations is avoided; (3) ages at which sizes are measured and maturation status are observed can differ between individuals. An application to data on the springtail Folsomia candida is presented. Models with age-dependent integration of maturation rates were preferred. The analysis demonstrates a significant size dependence of the maturation rate but no age dependence.     

Quantitative genetics of continuous reaction norms: thermal sensitivity of caterpillar growth rates

A continuous reaction norm or performance curve represents a phenotypic trait of an individual or genotype in which the trait value may vary with some continuous environmental variable. We explore patterns of genetic variation in thermal performance curves of short-term caterpillar growth rate in a population of Pieris rapae. We compare multivariate methods, which treat performance at each test temperature as a distinct trait, with function-valued methods that treat a performance curve as a continuous function. Mean growth rate increased with increasing temperatures from 8 to 35 degrees C, was highest at 35 degrees C, and declined at 40 degrees C. There was substantial and significant variation among full-sib families in their thermal performance curves. Estimates of broad-sense genetic variances and covariances showed that genetic variance in growth rate increased more than 30-fold from low (8-11 degrees C) to high (35-40 degrees C) temperatures, even after differences in mean growth rate across temperatures were removed. Growth rate at 35 and 40 degrees C was negatively correlated genetically, suggesting a genetic trade-off in growth rate at these temperatures; this trade-off may represent either a generalist-specialist trade-off and/or variation in the optimal temperature for growth. The estimated genetic variance-covariance function (G function), the function-valued analog of the variance-covariance matrix (G matrix), was quite bumpy compared with the estimated G matrix; and results of principal component analyses of the G function were difficult to interpret. The use of orthogonal polynomials as the basis functions in current function-valued estimation methods may generate artifacts when the true G function has prominent local features, such as strong negative covariances at nearby temperatures (e.g. at 35 and 40 degrees C); this may be a particular issue for thermal performance curves and other highly nonlinear reaction norms.     

Rapid population divergence in thermal reaction norms for an invading species: breaking the temperature-size rule

The temperature-size rule is a common pattern of phenotypic plasticity in which higher temperature during development results in a smaller adult body size (i.e. a thermal reaction norm with negative slope). Examples and exceptions to the rule are known in multiple groups of organisms, but rapid population differentiation in the temperature-size rule has not been explored. Here we examine the genetic and parental contributions to population differentiation in thermal reaction norms for size, development time and survival in the Cabbage White Butterfly Pieris rapae, for two geographical populations that have likely diverged within the past 150 years. We used split-sibship experiments with two temperature treatments (warm and cool) for P. rapae from Chapel Hill, NC, and from Seattle, WA. Mixed-effect model analyses demonstrate significant genetic differences between NC and WA populations for adult size and for thermal reaction norms for size. Mean adult mass was 12-24% greater in NC than in WA populations for both temperature treatments; mean size was unaffected or decreased with temperature (the temperature-size rule) for the WA population, but size increased with temperature for the NC population. Our study shows that the temperature-size rule and related thermal reaction norms can evolve rapidly within species in natural field conditions. Rapid evolutionary divergence argues against the existence of a simple, general mechanistic constraint as the underlying cause of the temperature-size rule.     

Comparative study of thermal reaction norms for development in ants

This is the first compilation of our research and data from the literature on the duration and thermal reaction norms for development in ants. Altogether, 97 regression lines characterizing the linear dependence of ant brood (egg, larval, prepupal and pupal) development on temperature were obtained for 33 species from 15 genera and three subfamilies. Significant positive correlations between the durations of different immature stages were revealed. We found differences between thermal reaction norms for development for various immature stages, some taxonomic groups, and southern and northern groups of species. All immature stages appeared to be shorter on average at 25°C in northern ants compared to southern species; this difference is insignificant only for eggs. Highly significant negative correlations were revealed between the temperature threshold for development (TTD) and the sum of degree‐days (SDD) for all immature stages. The latitudinal trends in intraspecific variation of thermal constants appeared to be opposite to those we observed at the interspecific level. At the latter, the coefficient of thermal sensitivity of development (i.e. the coefficient of linear regression of development rate on temperature) and TTD tends to decrease and SDD to increase from the south to the north. In contrast, at the intraspecific level, development became more temperature‐sensitive in northern populations, i.e. characterized by higher slopes of regression lines of development rate on temperature, and higher TTDs. The species of the genus Formica are characterized by the shortest and the most temperature‐sensitive immature development among all the ant species studied.     

Measuring probabilistic reaction norms for age and size at maturation

We present a new probabilistic concept of reaction norms for age and size at maturation that is applicable when observations are carried out at discrete time intervals. This approach can also be used to estimate reaction norms for age and size at metamorphosis or at other ontogenetic transitions. Such estimations are critical for understanding phenotypic plasticity and life-history changes in variable environments, assessing genetic changes in the presence of phenotypic plasticity, and calibrating size- and age-structured population models. We show that previous approaches to this problem, based on regressing size against age at maturation, give results that are systematically biased when compared to the probabilistic reaction norms. The bias can be substantial and is likely to lead to qualitatively incorrect conclusions; it is caused by failing to account for the probabilistic nature of the maturation process. We explain why, instead, robust estimations of maturation reaction norms should be based on logistic regression or on other statistical models that treat the probability of maturing as a dependent variable. We demonstrate the utility of our approach with two examples. First, the analysis of data generated for a known reaction norm highlights some crucial limitations of previous approaches. Second, application to the northeast arctic cod (Gadus morhua) illustrates how our approach can be used to shed new light on existing real-world data.     

Disentangling thermal preference and the thermal dependence of movement in ectotherms

Many ectotherms thermoregulate by choosing environmental temperatures that maximize diverse performance traits, including fitness. For this reason, physiological ecologists have measured preferred temperatures of diverse ectotherms for nearly a century. Thermal preference is usually measured by observing organism distributions on laboratory thermal gradients. This approach is appropriate for large ectotherms which have sufficient thermal inertia to decouple body temperatures from gradient temperatures. However, body temperatures and therefore speeds of movement of small ectotherms will closely track gradient temperature, making it difficult to distinguish between thermal preference and thermal dependence of movement. Here we develop and demonstrate the use of a patch model to derive the expected thermal gradient distribution given only the thermal dependence of movement. Comparison of this null distribution with the observed gradient distribution reveals thermal preference of small ectotherms.