In an earlier characterization of the relationship between morphology, performance and fitness, I focused only on directional selection (Arnold, 1983). The aim of this article is to extend that characterization to include stabilizing and other forms of nonlinear selection. As in the earlier characterization, this more general description of the morphology-performance-fitness relationship splits empirical analysis into two parts: the study of the relationship between morpholgy and performance, and the study of the relationship between performance and fitness. From a conceptual standpoint, my goal is to specify the relationship of performance studies to the adaptive landscape. I begin by reviewing the adaptive landscape concept and its importance in evolutionary biology. A central point emerging from that review is that that key descriptors of the adaptive landscape can be estimated by measuring the impact of selection on the means, variances and covariances of phenotypic traits. Those descriptors can be estimated by making a quadratic (regression) approximation to the selection surface that describes the relationship between the phenotypic traits of individuals and their fitness. Analysis of the effects of morphology on performance follows an analogous procedure: making a quadratic approximation to the individual performance surface and then using that approximation to solve for the descriptors of the performance landscape. I conclude by discussing the evolution of performance and adaptive landscapes. One possibility with biomechanical justification is that the performance landscape evolves along performance lines of least resistance.

Complex organismal traits such as body size are influenced by innumerable selective pressures, making the prediction of evolutionary trajectories for those traits difficult. A potentially powerful way to predict fitness in natural systems is to study the composite response of individuals in terms of performance measures, such as foraging or reproductive performance. Once key performance measures are identified in this top-down approach, we can determine the underlying physiological mechanisms and gain predictive power over long-term evolutionary processes. Here we use marine iguanas as a model system where body size differs by more than one order of magnitude between island populations. We identified foraging efficiency as the main performance measure that constrains body size. Mechanistically, foraging performance is determined by food pasture height and the thermal environment, influencing intake and digestion. Stress hormones may be a flexible way of influencing an individual's response to low-food situations that may be caused by high population density, famines, or anthropogenic disturbances like oil spills. Reproductive performance, on the other hand, increases with body size and is mediated by higher survival of larger hatchlings from larger females and increased mating success of larger males. Reproductive performance of males may be adjusted via plastic hormonal feedback mechanisms that allow individuals to assess their social rank annually within the current population size structure. When integrated, these data suggest that reproductive performance favors increased body size (influenced by reproductive hormones), with an overall limit imposed by foraging performance (influenced by stress hormones). Based on our mechanistic understanding of individual performances we predicted an evolutionary increase in maximum body size caused by global warming trends. We support this prediction using specimens collected during 1905. We also show in a common-garden experiment that body size may have a genetic component in iguanids. This ‘performance paradigm’ allows predictions about adaptive evolution in natural populations.

The morphology-performance-fitness paradigm is usually explored by determining whether natural or “phenotypically engineered” variation among individuals in morphology (physiology) or performance covaries with an index of fitness such as survival. Here we study between-line covariation between performance and fitness for 44 lines of flies that had undergone mutation accumulation (in the absence of natural selection) on the second chromosome for 62 generations, plus 13 control lines. These mutation accumulation (MA) lines were known to have reduced competitive fitness and life history scores, and to have positive between-line covariances among life history traits. We measured several performance traits of larvae and adults (and a life history trait), examined covariances among those trait means, and also examined covariances of traits with competitive fitness. MA lines had significantly lower performances than did control lines in most traits. However, because control lines had been unknowingly contaminated, a conclusion that MA reduces performance must be tentative. Correlations among performance traits were highly variable in sign, suggesting that MA does not negatively affect all traits equivalently. Even so, correlation matrices for MA and for control lines were very similar. In bivariate comparisons, only one performance trait (a “get-a-grip index,” which measures the ability of a falling fly to catch itself on baffles) was positively correlated with competitive fitness. Multivariate analyses again suggested the importance primarily of get-a-grip. Two main patterns emerge from this study. First, MA negatively affects diverse aspects of physiological performance, but does so differentially across traits. Second, except for GAG, MA-induced variation in performance is at best weakly correlated with competitive fitness.

Significant relationships among morphology, behavior, performance and fitness have long served as bona fide evidence for the role of selection in shaping natural populations. Here, I discuss how studies of ecological performance, or how organisms perform in nature, provide an ecological context for such selection studies. Laboratory studies assume that the level of performance expressed under “optimal” conditions accurately reflects the level of performance used in nature, but I show here that this assumption is not always borne out. A review of how various factors affect ecological performance (ontogeny, microhabitat, and macrohabitat) show that animals often express very different levels of movement speed both among different tasks, and when comparing laboratory versus field performance. Thus, a failure to take this variation into account could lead to negative, or even misleading significant fitness-character correlations. While laboratory performance studies should continue to play a key role in studies of selection, recent technological (i.e., portable high-speed cameras) and methodological developments should enable researchers to measure performance in nature to high degrees of accuracy. Thus, I encourage researchers to measure performance both in the laboratory and in the field, and thus expand the traditional paradigm of morphology → performance → fitness to morphology → ecological performance → fitness.

Coevolutionary interactions depend upon a phenotypic interface of traits in each species that mediate the outcome of interactions among individuals. These phenotypic interfaces usually involve performance traits, such as locomotion or resistance to toxins, that comprise an integrated suite of physiological, morphological and behavioral traits. The reciprocal selection from species interactions may act directly on performance, but it is ultimately the evolution of these underlying components that shape the patterns of coevolutionary adaptation in performance. Bridging the macroevolutionary patterns of coevolution to the ecological processes that build them therefore requires a way to dissect the phenotypic interface of coevolution and determine how specific components of performance in one species exert selection on complimentary components of performance in a second species. We present an approach for analyzing the strength of selection in a coevolutionary interaction where individuals interact at random, and for identifying which component traits of the phenotypic interface are critical to mediating coevolution. The approach is illustrated with data from a predator-prey arms race between garter snakes and newts that operates through the interface of tetrodotoxin (TTX) and resistance to it.

Ontogenetic conflict arises when optima for alleles governing fitness variation differ between juveniles and adults or between adult sexes. Loci that govern development of alternative phenotypes in the sexes, hereafter termed morph-determining loci, mediate development through the endocrine system. Morphotypic selection is defined to be multivariate selection favoring discrete alternative morphotypes (e.g., optima). When the optimal combinations of alleles for alternative morphs differ between the sexes, it generates conflicting selection pressure and thus ontogenetic conflict. Selection on morph alleles promotes ontogenetic conflict because it perturbs physiological epistasis that governs the expression of male versus female traits. Expression of physiological traits arises from homeostasis that maintains trait expression within a normal range. The genetic basis of homeostasis is likely to arise from interactions among several genes (e.g., genetic epistasis) or protein products (e.g., physiological epistasis). For example, endocrine regulation arises from interactions between gondatropins, which are protein hormones produced by the hypothalamic-pituitary glands, and steroid hormones, which are produced by the gonads (e.g., HPG axis). The side-blotched lizard system is discussed with respect to physiological bases of ontogenetic conflict. We also describe a novel molecular marker strategy for uncovering genome-wide physiological epistasis in nature. Finally, ontogenetic conflict exerts selection on females to evolve mate selection or cryptic choice that is reflected in different sires being chosen for son versus daughter production. We describe how side-blotched lizard females ameliorate ontogenetic conflict by cryptic choice of male genotypes to produce sons versus daughters.

Whole organism performance represents the integration of numerous physiological, morphological, and behavioral traits. How adaptive changes in performance evolve therefore requires an understanding of how selection acts on multiple integrated traits. Two approaches that lend themselves to studying the evolution of performance in natural populations are the use of quantitative genetics models for estimating the strength of selection acting on multiple quantitative traits and ecological genetic comparisons of populations exhibiting phenotypic differences correlated with environmental variation. In both cases, the ultimate goal is to understand how suites of traits and trade-offs between competing functions respond to natural selection. Here we consider how these two complimentary approaches can be applied to study the adaptive evolution of escape performance in fish. We first present an extension of Arnold's (1983) quantitative genetic approach that explicitly considers how trade-offs between different components of performance interact with the underlying genetics. We propose that such a model can reveal the conditions under which multiple selection pressures will cause adaptive change in traits that influence more than one component of fitness. We then review work on the Atlantic silversides and Trinidadian guppies as two case studies where an ecological genetics approach has been successfully applied to evaluate how the evolution of escape performance trades-off with other components of fitness. We conclude with the general lesson that whole organism performance is embedded in a complex phenotype, and that the net outcome of selection acting on different aspects of the organism will often result in a compromise among competing influences.

Invasive species that penetrate habitat boundaries are likely to experience strong selection and rapid evolution. This study documents evolutionary shifts in tolerance and performance following the invasion of fresh water by the predominantly estuarine and salt marsh copepod Eurytemora affinis. Common-garden experiments were performed on freshwater-invading (Lake Michigan) and ancestral saline (St. Lawrence marsh) populations to measure shifts in adult survival (at 0, 5, and 25 PSU), and survival during development and development time (both using full-sib clutches split across 0, 5, 15, and 25 PSU). Results showed clear evidence of heritable shifts in tolerance and performance associated with freshwater invasions. The freshwater population exhibited a gain in low-salinity tolerance and a reduction in high-salinity tolerance relative to the saline population, suggesting tradeoffs. These tradeoffs were supported by negative genetic correlations between survival at fresh (0 PSU) versus higher salinities. Mortality in response to salinity occurred primarily before metamorphosis, suggesting that selection in response to salinity had acted primarily on the early life-history stages. The freshwater population exhibited curious patterns of life-history evolution across salinities, relative to the saline population, of retarded development to metamorphosis but accelerated development from metamorphosis to adulthood. This pattern might reflect tradeoffs between development rate and survival in fresh water at the early life-history stages, but some other selective force acting on later life-history stages. Significant effects of clutch (genotype) and clutch-by-salinity interaction (G × E) on survival and development time in both populations indicated ample genetic variation as substrate for natural selection. Variation for high-salinity tolerance was present in the freshwater population despite negative genetic correlations between high- and low-salinity tolerance. Results implicate the importance of natural selection and document the evolution of reaction norms during freshwater invasions.

Functional challenges can differ among life-history stages, yet performance at one stage may be linked to the outcome of performance at others. For example, adult performance, in terms of the location or timing of reproduction in response to environmental signals, can set conditions that affect the performance of developmental stages. In marine invertebrates, however, early performance has been studied primarily in the laboratory. I outline an integrative approach to the study of field reproductive performance in a marine gastropod that undergoes development in intertidal habitats. Embryos within gelatinous masses experience high variability in development temperature and frequent exposure to thermal stress. In laboratory experiments, developmental performance was measured as a function of maximum temperature (T_max) experienced during fluctuations that mimicked field tidal profiles. Performance curves showed declines that coincided with temperature thresholds for heat shock protein (Hsp) expression, a signal of cellular stress. Application of laboratory results to field records of T_max predicted large variation in the survival of embryos deposited on different days. Timing of field reproduction was non-random with respect to T_max, suggesting that adults could help to buffer embryos from environmental stress. Embryo survival, however, was not predicted to benefit from the non-random pattern of adult reproduction. Adults may be constrained to respond to information that only weakly predicts conditions that embryos will experience. Studies that incorporate linkages between life cycle stages in the field may better reveal how performance capacities and constraints at one stage can influence performance and selection at others.

Many plants display a characteristic suite of developmental “shade avoidance” responses, such as stem elongation and accelerated reproduction, to the low ratio of red to far-red wavelengths (R:FR) reflected or transmitted from green vegetation. This R:FR cue of crowding and vegetation shade is perceived by the phytochrome family of photoreceptors. Phytochrome-mediated responses provide an ideal system for investigating the adaptive evolution of phenotypic plasticity in natural environments. The molecular and developmental mechanisms underlying shade avoidance responses are well studied, and testable ecological hypotheses exist for their adaptive significance. Experimental manipulation of phenotypes demonstrates that shade avoidance responses may be adaptive, resulting in phenotypes with high relative fitness in the environments that induce those phenotypes. The adaptive value of shade avoidance depends upon the competitive environment, resource availability, and the reliability of the R:FR cue for predicting the selective environment experienced by an induced phenotype. Comparative studies and a reciprocal transplant experiment with Impatiens capensis provide evidence of adaptive divergence in shade avoidance responses between woodland and clearing habitats, which may result from population differences in the frequency of selection on shade avoidance traits, as well as differences in the reliability of the R:FR cue. Recent rapid progress in elucidating phytochrome signaling pathways in the genetic model Arabidopsis thaliana and other species now provides the opportunity for studying how selection on shade avoidance traits in natural environments acts upon the molecular mechanisms underlying natural phenotypic variation.

Many aspects of physiological and organismal performance vary with some continuous environmental variable: e.g., photosynthetic rate as a function of light intensity; growth rate or sprint speed as a function of temperature. For such ‘performance curves’, the environment plays two roles: it affects both the levels of performance expressed, and the relationship between performance and fitness. How does environmental variation within a generation determine natural selection on performance curves? We describe an approach to this question that has three components. First, we quantify natural environmental variation and assess its impact on performance in the field. Second, we develop a simple theoretical model that predicts how fine-grained environmental variation determines selection on performance curves. Third, we describe how directional selection on performance curves may be estimated and compared to theoretical predictions. We illustrate these steps using data on performance curves of short-term growth rate as a function of temperature (thermal performance curves) in Pieris caterpillars. We use this approach to explore whether selection acts primarily on growth rate at specific temperatures, or on more integrated aspects of growth.