Joel G. Kingsolver

The Strength of Phenotypic Selection in Natural Populations

How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for studies that estimated the strength of linear and quadratic selection in terms of standardized selection gradients or differentials on natural variation in quantitative traits for field populations. We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. The absolute values of linear selection gradients |β| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon. The values of |β| for selection on morphological and on life‐history/phenological traits were significantly different: on average, selection on morphology was stronger than selection on phenology/life history. Similarly, the values of |β| for selection via aspects of survival, fecundity, and mating success were significantly different: on average, selection on mating success was stronger than on survival. Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. The absolute values of quadratic selection gradients |γ| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. The distribution of γ values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature.

Evolution of thermal sensitivity of ectotherm performance

Most ectothermal animals have variable body temperatures. Because physiological rates are temperature sensitive, an ectotherms behavioural and ecological performance - even its fitness - can be influenced by body temperature. As a result, the thermal sensitivity of ectotherm performance is relevant to diverse issues in physiology, ecology and evolution. This review formalizes an emerging framework for investigating the evolution of thermal sensitivity, outlines some functional and genetical constraints on that evolution, and summarizes comparative and experimental advances in this field.

Evolution of Resistance to High Temperature in Ectotherms

Body temperature influences the performance and fitness of ectotherms. How thermal sensitivity responds to selection for resistance to high temperature is broadly relevant in evolutionary physiology and also has practical implications. We review several complementary approaches to studying the evolution of thermal sensitivity. First, we analyze comparative data that illustrate the historical evolution of thermal sensitivity of locomotion in iguanid lizards. Taxa that experience high body temperatures in nature have evolved high optimal temperatures for sprinting. Critical thermal maxima are co-adapted with optimal temperatures but not with critical thermal minima. Thus some but not all aspects of thermal sensitivity are co-adapted. Second, we describe selection experiments that help reveal potential genetic constraints on the future evolution of thermal sensitivity in Drosophila. Thermal sensitivity responds rapidly both to laboratory natural selection and artificial selection, and tolerance of extreme high temperature appears genetically correlated with performance at intermediate temperature. Third, applying a recent model by Lynch and Lande, we describe how the shape of thermal performance curves may affect evolutionary responses of thermal sensitivity to a gradual shift in the thermal environment. Our theoretical predictions depend crucially on the relationship between the genetic variation in optimal temperature and the performance breadth. If genetic variation is independent of breadth, then populations with an intermediate value of performance breadth will tolerate the greatest rate of environmental change. Moreover, if a trade-off exists between maximum performance and breadth of performance, then thermal specialists will be favored over thermal generalists in a rapidly changing environment. On the other hand, if genetic variation increases with increasing breadth, then populations of thermal generalists will tolerate the greatest rates of environmental change.

Strength and tempo of directional selection in the wild

Directional selection is a major force driving adaptation and evolutionary change. However, the distribution, strength, and tempo of phenotypic selection acting on quantitative traits in natural populations remain unclear across different study systems. We reviewed the literature (1984–1997) that reported the strength of directional selection as indexed by standardized linear selection gradients (β). We asked how strong are viability and sexual selection, and whether strength of selection is correlated with the time scale over which it was measured. Estimates of the magnitude of directional selection (|β|) were exponentially distributed, with few estimates greater than 0.50 and most estimates less than 0.15. Sexual selection (measured by mating success) appeared stronger than viability selection (measured by survival). Viability selection that was measured over short periods (days) was typically stronger than selection measured over longer periods (months and years), but the strength of sexual selection did not vary with duration of selection episodes; as a result, sexual selection was stronger than viability selection over longer time scales (months and years), but not over short time scales (days).

INDIVIDUAL-LEVEL SELECTION AS A CAUSE OF COPE'S RULE OF PHYLETIC SIZE INCREASE

Abstract Copes rule, the tendency for species within a lineage to evolve towards larger body size, has been widely reported in the fossil record, but the mechanisms leading to such phyletic size increase remain unclear. Here we show that selection acting on individual organisms generally favors larger body size. We performed an analysis of the strength of directional selection on size compared with other quantitative traits by evaluating 854 selection estimates from 42 studies of contemporaneous natural populations. For size, more than 79% of selection estimates exceed zero, whereas for other morphological traits positive and negative values are similar in frequency. The selective advantage of increased size occurs for traits implicated in both natural selection (e.g., differences in survival) and sexual selection (e.g., differences in mating success). The predominance of positive directional selection on size within populations could translate into a macroevolutionary trend toward increased size and thereby explain Copes rule.

The Well‐Temperatured Biologist

Temperature provides a powerful theme for exploring environmental adaptation at all levels of biological organization, from molecular kinetics to organismal fitness to global biogeography. First, the thermodynamic properties that underlie biochemical kinetics and protein stability determine the overall thermal sensitivity of rate processes. Consequently, a single quantitative framework can assess variation in thermal sensitivity of ectotherms in terms of single amino acid substitutions, quantitative genetics, and interspecific differences. Thermodynamic considerations predict that higher optimal temperatures will result in greater maximal fitness at the optimum, a pattern seen both in interspecific comparisons and in within‐population genotypic variation. Second, the temperature‐size rule (increased developmental temperature causes decreased adult body size) is a common pattern of phenotypic plasticity in ectotherms. Mechanistic models can correctly predict the rule in some taxa, but lab and field studies show that rapid evolution can weaken or even break the rule. Third, phenotypic and evolutionary models for thermal sensitivity can be combined to explore potential fitness consequences of climate warming for terrestrial ectotherms. Recent analyses suggest that climate change will have greater negative fitness consequences for tropical than for temperate ectotherms, because many tropical species have relatively narrow thermal breadths and smaller thermal safety margins.

Path analyses of selection

Identifying the targets and causal mechanisms of phenotypic selection in natural populations remains an important challenge for evolutionary biologists. Path analysis is a statistical modeling approach that may aid in meeting this challenge. We describe several types of path model that are relevant to the analysis of selection, and review some recent empirical studies that apply path models to issues in pollination biology, phenotypic integration and selection on morphometric and ontogenetic traits. Path analysis may play two roles in the analysis of selection: first, as an exploratory analysis suggesting possible targets of selection, which are then tested by direct experimentation; and second, as a means of evaluating the relative importance of different causal pathways of selection, once the likely targets of selection have been established.

THERMOREGULATORY STRATEGIES IN COLIAS BUTTERFLIES: THERMAL STRESS AND THE LIMITS TO ADAPTATION IN TEMPORALLY VARYING ENVIRONMENTS

As a case study of adaptive strategies in temporally varying environments, thermoregulation in three populations of Colias butterflies along an elevation gradient in Colorado is studied in relation to the fluctuating meteorological environment. Emphasis is placed on short time scale (15-300 s) variation in air temperature and wind speed and its role in determining elevational patterns of body temperature, flight activity, and thermal stress due to overheating. A stochastic, linear filter model of an organism in a variable environment is used which views the adaptive process as the adjustment of the organisms filter. The relation-ship between this filter model and a transient energy balance model of the butterfly is examined to show how the thermoregulatory mechanisms of adaptation determine the filtering properties of the organism. Heat shocks at 45⚬ C significantly decrease survivorship and fecundity in Colias. Time series analysis indicates that short-term variation in wind speed and air temperature under sunny, midday conditions is significantly greater at higher elevation sites. Negative cross-correlations between wind speed and air temperature at certain time scales amplify the probability of overheating in Colias. Simulation and field results show that Colias from higher elevation populations are more sensitive, in terms of body temperature response, to a given level of wind speed variability, because of their higher wing solar absorptivities. As a result of these factors, variation in body temperature under sunny, midday conditions is significantly greater for butterflies in higher elevation Colias populations, regardless of behavioral thermoregulation. While mean body temperatures under these conditions are 2⚬ C-3⚬ C higher for low elevation than for high elevation Colias, the maximum body temperatures experienced in these populations are similar. These results are consistent with the hypothesis that microevolution of thermoregulatory characteristics in Colias is constrained by the need to avoid high body temperatures. The differences in mean body temperatures which follow from this constraint and the elevational differences in meteorological variation may be a major factor in the elevational patterns of daily flight activity time observed in previous studies. By documenting the biological importance of thermal stress and flight activity for Colias, we can develop optimality models for thermoregulatory strategy. To our knowledge, this is the first comprehensive demonstration of quantitative differences in environmental variability and their consequences for differences in adaptive characteristics among animal populations. Results are discussed in relation to strategies of insect thermoregulation, the structure of the micromete-orological environment, and general principles of adaptive design in variable environments.

Complex Life Cycles and the Responses of Insects to Climate Change

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

Patterns and Power of Phenotypic Selection in Nature

ABSTRACT Phenotypic selection occurs when individuals with certain characteristics produce more surviving offspring than individuals with other characteristics. Although selection is regarded as the chief engine of evolutionary change, scientists have only recently begun to measure its action in the wild. These studies raise numerous questions: How strong is selection, and do different types of traits experience different patterns of selection? Is selection on traits that affect mating success as strong as selection on traits that affect survival? Does selection tend to favor larger body size, and, if so, what are its consequences? We explore these questions and discuss the pitfalls and future prospects of measuring selection in natural populations.