Whole-organism Performance Traits Research Articles

Sex- and trait-specific silver-spoon effects of developmental environments, on ageing

The environment organisms experience during development can have effects which carry over into their adult lives. These environments not only affect adult traits at a given point in time, but also how these traits change with age. Generally, favorable developmental environments lead to more optimal adult traits while stressful environments are deleterious (“silver-spoon effect”). But whether developmental environments affect how whole-organism performance traits change with age or whether they affect males and females differently lacks evidence. Here, we test whether experiencing favorable developmental environments leads to “silver-spoon effects” on life-history traits and whole-organism flight performance of males and females by manipulating developmental density in Callosobruchus maculatus. We further test whether such effects are mediated by an individual’s reproductive status by comparing traits of mated versus virgin females. We show that although developmental crowding has no effect on flight performance of either sex, on male adult lifespan, or on female age-dependent survival, it is detrimental to female lifespan and fecundity, as well as female age-dependent reproduction, suggesting that females are more sensitive to differences in developmental density. Additionally, we show that flight traits change with age and differ not only between males and females, which is reflective of sex-specific life-histories and behavior, but also between virgin and mated females. Our study is important for understanding sex-specific responses to developmental environments in life-history, behavioral, and ecologically important traits which may affect resource allocation, dispersal, and mating strategies, hence fitness.

Refining the activity level-predation risk paradigm in larval anuran communities

The activity level-predation risk paradigm of community assembly is based on observable trade-offs between activity level and predation risk. Many species that live in ephemeral habitats are relatively more active, grow faster, and metamorphose sooner than those in more permanent habitats, thus enabling them to survive by escaping drying ponds. Species with high activity levels are shown to be superior competitors in temporary ponds, but are at greater risk of predation by visually cued predators. We take a comprehensive approach to testing if the activity-predation paradigm drives community assembly of a four-species guild of larval anurans through field surveys and a series of laboratory experiments quantifying their activity level, anti-predatory responses, swim performance, and escape behavior. Activity level was a good predictor of susceptibility to predation and habitat association for most species in our study, but not all species fit the pattern. Secondary anti-predator mechanisms contributed to differences in susceptibility to predation. Some species were more capable of avoiding predation through swim performance and escape behavior, thus allowing them to occupy a greater range of the water permanency continuum than was predicted by activity level alone. Because performance traits are deeply rooted, evolutionary history plays a major role in determining tadpole performance and life-history traits. Whole-organism performance traits (e.g., swim performance, escape behavior) have not generally been considered in the classic activity-predation paradigm. Our results show that accounting for individual and species-level performance reveals the understudied, yet important role of species-specific performance traits in disentangling the mechanisms driving community assembly.

Conflict, compensation, and plasticity: Sex-specific, individual-level trade-offs in green anole (Anolis carolinensis) performance.

Trade-offs in performance expression occur because animals must perform multiple whole-organism performance tasks that place conflicting demands on shared underlying morphology. Although not always detectable within populations, such trade-offs may be apparent when analyzed at the level of the individual, particularly when all of the available data are taken into account as opposed to only maximum values. Detection of performance trade-offs is further complicated in species where sexual dimorphism drives performance differences between males and females, leading potentially to differing patterns of trade-offs within each sex. We tested for within- and between-individual trade-offs among three whole-organism performance traits (sprint speed, endurance, and bite force) in adult male and female Anolis carolinensis lizards using all of the measured performance data. Sprinting and endurance did not trade-off among individuals in either sex, but we found a significant negative among-individual relationship between sprint speed and bite force in females only, likely driven by the mechanical burden of larger than optimal heads imposed on females through intralocus sexual conflict. We also found evidence for marked within-individual plasticity in male bite force, but no within-individual trade-offs between any traits in either sex. These data offer new insight into the sex-specific nature of performance trade-offs and plasticity and, ultimately, into the constraints on multivariate performance evolution.

Predicting Life-History Trade-Offs with Whole-Organism Performance.

Whole-organism performance traits are key intermediaries between the organism and the environment. Because performance traits are energetically costly to both build and maintain, performance will compete with other life-history traits over a limited pool of acquired energetic resources at any given time, potentially leading to trade-offs in performance expression. Although these trade-offs can have important implications for organismal fitness we currently lack a conceptual framework for predicting both where trade-offs might be expected, and which traits may be especially prone to trade-offs with other fitness-related life-history traits. We propose such a framework based on an estimate of the energetic requirements of locomotion in vertebrates, the ecological cost of transport. By analyzing existing data on mammalian energetic budgets and life-history, we found that species with higher costs of locomotion also tended to be those with "slow" life histories that invest relatively less in current reproduction than "fast" life-history species. We discuss the potential implications of ectothermy for masking such relationships, and how this framework might be expanded upon in the future.

Introduction to the Symposium: Integrative Life-History of Whole-Organism Performance.

A strong case can be made for whole-organism performance traits (i.e., dynamic, ecologically relevant traits whose expression is shaped by underlying morphological factors) as being the ultimate integrative traits. This is not only because they capture the output of multiple lower levels of biological organization, but also because they are directly relevant to individual fitness in multiple ecological contexts, and are in many cases important proximate determinants of survival and/or reproductive success. But although many ecological and evolutionary phenomena can be examined through the lens of performance (and vice-versa), performance research has been surprisingly slow to incorporate concepts from the large and important field of life-history evolution. Such a synthesis is necessary, because shifts in resource allocation strategies can have implications for these highly ecologically relevant, functional traits, whose expression may trade-off against fecundity, immune function, or longevity, among other key life-history traits. The papers in this symposium showcase many of the ways in which life-history strategies can have direct consequences for the expression, maintenance, and evolution of whole-organism performance (and at least one case where they may not). By approaching the issue of life-history trade-offs from a number of diverse perspectives, this symposium reveals the scope for future explicit integration of life-history techniques with those of whole-organism performance studies for a more complete understanding of multivariate phenotypic evolution.

How Do We Measure the Cost of Whole-Organism Performance Traits?

Whole-organism performance traits, such as maximal speed and endurance capacity are undoubtedly costly, but we know little about how or when all of the costs associated with performance are paid to individuals or how to measure them. To understand how performance traits might be involved in trade-offs with other life-history traits it is critical to determine the development, production, and maintenance costs of performance traits, as well as how each of these changes with increased or decreased use of the performance trait. We discuss the advantages and disadvantages of several potential phenotypic measures of dynamic whole-organism performance that may be used in life-history studies, including direct performance measures; metabolic rates; ecological cost of transport; and changes in metabolic rate after training. We use the first approach, direct performance measures, to show trade-offs between endurance capacity and several traditional life history variables in phrynosomatid lizards. The largest problem currently in determining the costs of performance traits and how those costs might lead to life-history trade-offs is that there are estimates of performance costs in very few taxa, and when there are, those species typically are not studied with respect to "traditional" life-history traits.

Water Stress Affects Development Time but Not Takeoff Performance in the Butterfly Pararge aegeria.

Most organisms are limited in the amount and type of resources they are able to extract from the environment. The juvenile environment is particularly important in this regard, as conditions over ontogeny can influence the adult phenotype. Whole-organism performance traits, such as locomotion, are susceptible to such environmental effects, yet the specific biotic and abiotic factors driving performance plasticity have received little attention. We tested whether speckled wood Pararge aegeria L. butterflies reared under conditions of water stress exhibited poorer flight morphology and performance than control individuals. Despite large differences in mortality between treatments, we found no effects of water stress treatment on takeoff performance and only minor treatment effects on flight morphology. However, butterflies reared on water-stressed diets exhibited both significantly greater mortality and longer development times than did control individuals. Pararge aegeria larvae may compensate for this stress by prolonging development, resulting in similar realized performance capacities at least in takeoff performance in surviving adult butterflies; other measures of flight performance remain to be considered. Alternatively, the adult phenotype may be insulated from environmental effects at the larval stage in these insects.

An Individual-Based Simulation Approach to the Evolution of Locomotor Performance.

Maximal whole-organism performance traits measured in the laboratory and the levels of performance expressed in the field often exhibit a mismatch, complicating our understanding of the selection pressures influencing the evolution of performance traits. To better understand the evolution of locomotor performance, we built an individual-based simulation to test hypotheses about selection on locomotor performance. Starting with a population of individuals with two correlated but variable performance traits, we simulated these individuals surviving and reproducing in a complex environment, presenting each individual with successive ecological challenges requiring specific performance capabilities over their lifespan. While most challenges require sub-maximal speeds, intermittent bouts requiring increased performance, such as escape from predators, introduce strong, but infrequent, selection for maximal performance. By comparing the results of simulations run with individuals that only perform at their maximum levels versus those that adjust this effort, we show that intra-individual variation in speed confers a selective advantage, regardless of the extent of that variation. We also show that the direction and strength of the correlation between the two performance traits affects the evolutionary trajectory of phenotypic change. Ultimately, this model allows us to simulate the evolution of movement speeds over a range of selective contexts, offering insight into the factors affecting the evolutionary relationship between optimal and maximal performance.

The life history of whole-organism performance.

For almost 40 years, studies of whole-organism performance have formed a cornerstone of evolutionary physiology. Although its utility as a heuristic guide is beyond question, and we have learned much about morphological evolution from its application, the ecomorphological paradigm has frequently been applied to performance evolution in ways that range from unsatisfactory to inappropriate. More importantly, the standard ecomorphological paradigm does not account for tradeoffs among performance and other traits, nor between performance traits that are mediated by resource allocation. A revised paradigm that includes such tradeoffs, and the possible ways that performance and fitness-enhancing traits might affect each other, could potentially revivify the study of phenotypic evolution and make important inroads into understanding the relationships between morphology and performance and between performance and Darwinian fitness. We describe such a paradigm, and discuss the various ways that performance and key life-history traits might interact with and affect each other. We emphasize both the proximate mechanisms potentially linking such traits, and the likely ultimate factors driving those linkages, as well as the evolutionary implications for the overall, multivariate phenotype. Finally, we highlight several research directions that will shed light on the evolution and ecology of whole-organism performance and related life-history traits.

Running in cold weather: morphology, thermal biology, and performance in the southernmost lizard clade in the world (Liolaemus lineomaculatussection: Liolaemini: Iguania)

The integration or coadaptation of morphological, physiological, and behavioral traits is represented by whole-organism performance traits such as locomotion or bite force. Additionally, maximum sprint speed is a good indicator of whole-organism performance capacity as variation in sprinting ability can affect survival. We studied thermal biology, morphology, and locomotor performance in a clade of Liolaemus lizards that occurs in the Patagonian steppe and plateaus, a type of habitat characterized by its harsh cold climate. Liolaemus of the lineomaculatus section display a complex mixture of conservative and flexible traits. The phylogenetically informed analyses of these ten Liolaemus species show little coevolution of their thermal traits (only preferred and optimum temperatures were correlated). With regard to performance, maximum speed was positively correlated with optimum temperature. Body size and morphology influenced locomotor performance. Hindlimbs are key for maximal speed, but forelimb length was a better predictor for sustained speed (i.e. average speed over a total distance of 1.2 m). Finally, sustained speed differed among species with different diets, with herbivores running on average faster over a long distance than omnivores.

DIFFERENTIAL AGING OF BITE AND JUMP PERFORMANCE IN VIRGIN AND MATED TELEOGRYLLUS COMMODUS CRICKETS

Evolutionary theories of aging state that the force of natural selection declines with age, resulting in trait senescence. However, sexual selection theory predicts that costly traits that signal mate value should increase in expression as survival prospects decline. Mortality rates and fertility tend to show strong signatures of senescence, whereas sexual signaling traits increase with age, but how the expression of traits such as whole-organism performance measures that are subject to both sexual and nonsexual selection should change with age is unclear. We examined the effects of both a key life-history event (mating) and diet quality (male and female optimal diets) on aging in two whole-organism performance traits (bite force and jump take-off velocity) in male and female Teleogryllus commodus crickets. We found no evidence for diet effects on any of the measured traits. Aging effects were more evident in females than in males for both jumping and biting, and constitute a mix of senescence and terminal investment patterns depending on sex/mating class. Sex and mating therefore have important implications for resource allocation to performance traits, and hence for aging of those traits, and interactions between these two factors can result in complex changes in trait expression over individual lifetimes.

How does selection operate on whole-organism functional performance capacities? A review and synthesis

Hypothesis: Natural and sexual selection should be stronger on whole-organism functional performance traits (sprinting, biting) than on correlated morphological variables. Organisms: Lizards, snakes, turtles, frogs, and fish (review of past field and laboratory studies). Field sites: Various (review of past field and laboratory studies). Methods: We reviewed existing literature on the nature and intensity of natural and sexual selection on whole-organism performance traits. We answer some key questions in regards to how selection operates on performance, and whether selection is stronger on performance compared with morphological traits. Results: We identified 23 studies that have quantified selection on performance. Natural and sexual selection were typically directional in nature, with a distinct preference for high rather than low values of performance. However, some studies uncovered no significant selection on performance, and there was also no evidence that selection was stronger on performance traits than morphological traits.

Performance is no proxy for genetic quality: trade‐offs between locomotion, attractiveness, and life history in crickets

The genetic relationships among traits contributing to overall fitness are an important subject of inquiry because such relationships influence how suites of traits respond to selection. Within the field of sexual selection, these relationships are also of interest for assessing whether any given trait can be used as a proxy for total fitness. A growing number of studies have demonstrated close links between whole-organism performance traits and determinants of individual fitness; however, an understanding of the genetic relationships between performance and important aspects of genetic quality is currently lacking. We present the results of a quantitative genetic study in which we estimate covariation between a locomotor performance trait (maximal jumping ability), calling effort, sexual attractiveness, and life-history traits in male Teleogryllus commodus crickets. We show that the major axis of genetic variation (gmax) is characterized by a contrast between jump performance and life-history traits associated with mating success. Moreover, two additional axes of significant multivariate genetic variation exist, each characterized by strong contrasts among traits. These results argue against the existence of a single axis representing genetic quality, favoring instead the idea that resource allocation strategies shape multiple dimensions of genetic quality through trade-offs among key life-history traits, including performance.

NATURAL SELECTION REDUCES ENERGY METABOLISM IN THE GARDEN SNAIL,HELIX ASPERSA(CORNU ASPERSUM)

Phenotypic selection is widely recognized as the primary cause of adaptive evolution in natural populations, a fact that has been documented frequently over the last few decades, mainly in morphological and life-history traits. The energetic definition of fitness predicts that natural selection will maximize the residual energy available for growth and reproduction, suggesting that energy metabolism could be a target of selection. To address this problem, we chose the garden snail, Helix aspersa (Cornu aspersum). We performed a seminatural experiment for measuring phenotypic selection on standard metabolic rate (SMR), the minimum cost of maintenance in ectotherm organisms. To discount selection on correlated traits, we included two additional whole-organism performance traits (mean speed and maximum force of dislodgement). We found a combination of linear (negative directional selection, beta=-0.106 +/- 0.06; P= 0.001) and quadratic (stabilizing selection, gamma=-0.012 +/- 0.033; P= 0.061) selection on SMR. Correlational selection was not significant for any possible pair of traits. This suggests that individuals with average-to-reduced SMRs were promoted by selection. To the best of our knowledge, this is the first study showing significant directional selection on the obligatory cost of maintenance in an animal, providing support for the energetic definition of fitness.

Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animal performance measure

Measurements of whole-organism performance traits have been useful in studies of adaptation and phenotype– environment correlations. Bite force capacities may be tightly linked to both the type and magnitude of the ecological challenges of food acquisition, mate acquisition, and antipredation in vertebrates. In the present study, we present technical details on bite meters and on measuring bite forces. The ability to take reliable measurements depends on specific features of the measuring device and on where in the mouth the bite is applied. Using both previously available and original data, we demonstrate several ecologically and evolutionarily relevant features of bite force measurements. First, maximal bite forces are repeatable among individuals across all vertebrates studied to date. Second, in ectotherms such as lizards, maximal bite forces are affected by body temperature and motivational states. Third, bite forces are strongly correlated with head size and shape. Fourth, bite forces correlate with features of prey of vertebrates. Finally, bite forces are linked to male dominance and correlated with social-display structures. Thus, bite force performance measures can be used as ‘traits’, and thus be used in integrative studies at multiple levels of organismal biology. Accordingly, bite force data will help our understanding of the functions, capacities, and evolution of jaw–cranial musculoskeletal systems. Moreover, a plethora of opportunities exist for the use of bite force measurements, and if methods are carefully applied, several levels of organismal and ecological organization can be integrated to aid our understanding of the ecology and evolution of vertebrate taxa. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 709–720.

FAST FATHERS FATHER MORE

![Figure][1] It is widely assumed that in the animal kingdom faster means better. Speed often implies that an animal is better at escaping from predators, and capturing prey. Indeed, a growing number of studies are linking whole-organism performance traits, such as locomotor speed, to an

Gaping Displays Reveal and Amplify a Mechanically Based Index of Weapon Performance

Physical prowess, a key determinant of fight outcomes, is contingent on whole-organism performance traits. The advertisement of performance, via display, is poorly understood because it is unclear how information about performance is encoded into display characteristics. Previous studies have shown that weapon performance (i.e., bite force) predicts dominance and reproductive success in male lizards. We tested the hypothesis that gaping displays by adult male collared lizards (Crotaphytus) can provide an index of weapon performance by exposing the major jaw-adductor muscle complex and that white patches at the mouth corners amplify this index. For territorial adult males, the breadth of the muscle complex, which is not correlated with body size, was a strong predictor of bite force. For nonterritorial yearling males and females, however, measures of body and head size predicted bite force. The patches are highly conspicuous, exhibit UV-reflecting properties within the visual range of lizards, and provide size-independent information about bite force only in adult males. We conclude that exposure of the muscle complex during gaping displays can provide rival males with a reliable, body-size independent, biomechanically based index of weapon performance, an index that the mouth-corner patches amplify. Indexes that transmit information through mechanistic links to performance are expected to be widespread among animals.