Performance, personality, and energetics : correlation, causation, and mechanism

The study of phenotypic evolution should be an integrative endeavor that combines different approaches and crosses disciplinary and phylogenetic boundaries to consider complex traits and organisms that historically have been studied in isolation from each other. Analyses of individual variation within populations can act to bridge studies focused at the levels of morphology, physiology, biochemistry, organismal performance, behavior, and life history. For example, the study of individual variation recently facilitated the integration of behavior into the concept of a pace-of-life syndrome and effectively linked the field of energetics with research on animal personality. Here, we illustrate how studies on the pace-of-life syndrome and the energetics of personality can be integrated within a physiology-performance-behavior-fitness paradigm that includes consideration of ecological context. We first introduce key concepts and definitions and then review the rapidly expanding literature on the links between energy metabolism and personality traits commonly studied in nonhuman animals (activity, exploration, boldness, aggressiveness, sociability). We highlight some empirical literature involving mammals and squamates that demonstrates how emerging fields can develop in rather disparate ways because of historical accidents and/or particularities of different kinds of organisms. We then briefly discuss potentially interesting avenues for future conceptual and empirical research in relation to motivation, intraindividual variation, and mechanisms underlying trait correlations. The integration of performance traits within the pace-of-life-syndrome concept has the potential to fill a logical gap between the context dependency of selection and how energetics and personality are expected to interrelate. Studies of how performance abilities and/or aspects of Darwinian fitness relate to both metabolic rate and personality traits are particularly lacking.

Interplay among nocturnal activity, melatonin, corticosterone and performance in the invasive cane toad (Rhinella marinus)

Most animals conduct daily activities exclusively either during the day or at night. Here, hormones such as melatonin and corticosterone, greatly influence the synchronization or regulation of physiological and behavioral cycles needed for daily activity. How then do species that exhibit more flexible daily activity patterns, responses to ecological, environmental or life-history processes, regulate daily hormone profiles important to daily performance? This study examined the consequences of (1) nocturnal activity on diel profiles of melatonin and corticosterone and (2) the effects of experimentally increased acute melatonin levels on physiological and metabolic performance in the cane toad (Rhinella marinus). Unlike inactive captive toads that had a distinct nocturnal melatonin profile, nocturnally active toads sampled under field and captive conditions, exhibited decreased nocturnal melatonin profiles with no evidence for any phase shift. Nocturnal corticosterone levels were significantly higher in field active toads than captive toads. In toads with experimentally increased melatonin levels, plasma lactate and glucose responses following recovery post exercise were significantly different from control toads. However, exogenously increased melatonin did not affect resting metabolism in toads. These results suggest that toads could adjust daily hormone profiles to match nocturnal activity requirements, thereby avoiding performance costs induced by high nocturnal melatonin levels. The ability of toads to exhibit plasticity in daily hormone cycles, could have broad implications for how they and other animals utilize behavioral flexibility to optimize daily activities in response to natural and increasingly human mediated environmental variation.

Evolution of form and function: morphophysiological relationships and locomotor performance in tropidurine lizards

Locomotor capacity is often considered an excellent measure of whole animal performance because it requires the integrated functioning of many morphological, physiological (and biochemical) traits. However, because studies tend to focus on either structural or functional suits of traits, we know little on whether and how morphological and physiological traits coevolve to produce adequate locomotor capacities. Hence, we investigate the evolutionary relationships between morphological and physiological parameters related to exercise physiology, using tropidurine lizards as a model. We employ a phylogenetic principal component analysis (PCA) to identify variable clusters (factors) related to morphology, energetic metabolism and muscle metabolism, and then analyze the relationships between these clusters and measures of locomotor performance, using two models (star and hierarchical phylogenies). Our data indicate that sprint performance is enhanced by simultaneous evolutionary tendencies affecting relative limb and tail size and physiological traits. Specifically, the high absolute sprint speeds exhibited by tropidurines from the sand dunes are explained by longer limbs, feet and tails and an increased proportion of glycolytic fibers in the leg muscle, contrasting with their lower capacity for overall oxidative metabolism [principal component (PC1)]. However, when sprint speeds are corrected for body size, performance correlates with a cluster (PC3) composed by moderate loads for activity metabolic rate and body size. The simultaneous measurement of morphological and physiological parameters is a powerful tool for exploring patterns of coadaptation and proposing morphophysiological associations that are not directly predictable from theory. This approach may trigger novel directions for investigating the evolution of form and function, particularly in the context of organismal performance.

Predicting climate warming effects on green turtle hatchling viability and dispersal performance

Ectotherms are taxa considered highly sensitive to rapid climate warming. This is because body temperature profoundly governs their performance, fitness and life history. Yet, while several modelling approaches currently predict thermal effects on some aspects of life history and demography, they do not consider how temperature simultaneously affects developmental success and offspring phenotypic performance, two additional key attributes that are needed to comprehensively understand species responses to climate warming. Here, we developed a stepwise, individual-level modelling approach linking biophysical and developmental models with empirically derived performance functions to predict the effects of temperature-induced changes to offspring viability, phenotype and performance, using green sea turtle hatchlings as an ectotherm model. Climate warming is expected to particularly threaten sea turtles, as their life-history traits may preclude them from rapid adaptation. Under conservative and extreme warming, our model predicted large effects on performance attributes key to dispersal, as well as a reduction in offspring viability. Forecast sand temperatures produced smaller, weaker hatchlings, which were up to 40% slower than at present, albeit with increased energy stores. Conversely, increases in sea surface temperatures aided swimming performance. Our exploratory study points to the need for further development of integrative individual-based modelling frameworks to better understand the complex outcomes of climate change for ectotherm species. Such advances could better serve ecologists to highlight the most vulnerable species and populations, encouraging prioritization of conservation effort to the most threatened systems.

Flight metabolic rate in the Glanville fritillary butterfly

Dispersal is a highly important life history trait. In fragmented landscapes the long-term persistence of populations depends on dispersal. Evolution of dispersal is affected by costs and benefits and these may differ between different landscapes. This results in differences in the strength and direction of natural selection on dispersal in fragmented landscapes. Dispersal has been shown to be a nonrandom process that is associated with traits such as flight ability in insects. This thesis examines genetic and physiological traits affecting dispersal in the Glanville fritillary butterfly (Melitaea cinxia). Flight metabolic rate is a repeatable trait representing flight ability. Unlike in many vertebrates, resting metabolic rate cannot be used as a surrogate of maximum metabolic rate as no strong correlation between the two was found in the Glanville fritillary. Resting and flight metabolic rate are affected by environmental variables, most notably temperature. However, only flight metabolic rate has a strong genetic component. Molecular variation in the much-studied candidate locus phosphoglucose isomerase (Pgi), which encodes the glycolytic enzyme PGI, has an effect on carbohydrate metabolism in flight. This effect is temperature dependent: in low to moderate temperatures individuals with the heterozygous genotype at the single nucleotide polymorphism (SNP) AA111 have higher flight metabolic rate than the common homozygous genotype. At high temperatures the situation is reversed. This finding suggests that variation in enzyme properties is indeed translated to organismal performance. High-resolution data on individual female Glanville fritillaries moving freely in the field were recorded using harmonic radar. There was a strong positive correlation between flight metabolic rate and dispersal rate. Flight metabolic rate explained one third of the observed variation in the one-hour movement distance. A fine-scaled analysis of mobility showed that mobility peaked at intermediate ambient temperatures but the two common Pgi genotypes differed in their reaction norms to temperature. As with flight metabolic rate, heterozygotes at SNP AA111 were the most active genotype in low to moderate temperatures. The results show that molecular variation is associated with variation in dispersal rate through the link of flight physiology under the influence of environmental conditions. The evolutionary pressures for dispersal differ between males and females. The effect of flight metabolic rate on dispersal was examined in both sexes in field and laboratory conditions. The relationship between flight metabolic rate and dispersal rate in the field and flight duration in the laboratory were found to differ between the two sexes. In females the relationship was positive, but in males the longest distances and flight durations were recorded for individuals with low flight metabolic rate. These findings may reflect male investment in mate locating. Instead of dispersing, males with high flight metabolic rate may establish territories and follow a perching strategy when locating females and hence move less on the landscape level. Males with low metabolic rate may be forced to disperse due to low competitive success or may show adaptations to an alternative strategy: patrolling. In the light of life history trade-offs and the rate of living theory having high metabolic rate may carry a cost in the form of shortened lifespan. Experiments relating flight metabolic rate to longevity showed a clear correlation in the opposite direction: high flight metabolic rate was associated with long lifespan. This suggests that individuals with high metabolic rate do not pay an extra physiological cost for their high flight capacity, rather there are positive correlations between different measures of fitness. These results highlight the importance of condition.

Head shape evolution in Tropidurinae lizards: does locomotion constrain diet?

Different components of complex integrated systems may be specialized for different functions, and thus the selective pressures acting on the system as a whole may be conflicting and can ultimately constrain organismal performance and evolution. The vertebrate cranial system is one of the most striking examples of a complex system with several possible functions, being associated to activities as different as locomotion, prey capture, display and defensive behaviours. Therefore, selective pressures on the cranial system as a whole are possibly complex and may be conflicting. The present study focuses on the influence of potentially conflicting selective pressures (diet vs. locomotion) on the evolution of head shape in Tropidurinae lizards. For example, the expected adaptations leading to flat heads and bodies in species living on vertical structures may conflict with the need for improved bite performance associated with the inclusion of hard or tough prey into the diet, a common phenomenon in Tropidurinae lizards. Body size and six variables describing head shape were quantified in preserved specimens of 23 species, and information on diet and substrate usage was obtained from the literature. No phylogenetic signal was observed in the morphological data at any branch length tested, suggesting adaptive evolution of head shape in Tropidurinae. This pattern was confirmed by both factor analysis and independent contrast analysis, which suggested adaptive co-variation between the head shape and the inclusion of hard prey into the diet. In contrast to our expectations, habitat use did not constrain or drive head shape evolution in the group.

Evolution of Body Elongation in Gymnophthalmid Lizards: Relationships with Climate

The evolution of elongated body shapes in vertebrates has intrigued biologists for decades and is particularly recurrent among squamates. Several aspects might explain how the environment influences the evolution of body elongation, but climate needs to be incorporated in this scenario to evaluate how it contributes to morphological evolution. Climatic parameters include temperature and precipitation, two variables that likely influence environmental characteristics, including soil texture and substrate coverage, which may define the selective pressures acting during the evolution of morphology. Due to development of geographic information system (GIS) techniques, these variables can now be included in evolutionary biology studies and were used in the present study to test for associations between variation in body shape and climate in the tropical lizard family Gymnophthalmidae. We first investigated how the morphological traits that define body shape are correlated in these lizards and then tested for associations between a descriptor of body elongation and climate. Our analyses revealed that the evolution of body elongation in Gymnophthalmidae involved concomitant changes in different morphological traits: trunk elongation was coupled with limb shortening and a reduction in body diameter, and the gradual variation along this axis was illustrated by less-elongated morphologies exhibiting shorter trunks and longer limbs. The variation identified in Gymnophthalmidae body shape was associated with climate, with the species from more arid environments usually being more elongated. Aridity is associated with high temperatures and low precipitation, which affect additional environmental features, including the habitat structure. This feature may influence the evolution of body shape because contrasting environments likely impose distinct demands for organismal performance in several activities, such as locomotion and thermoregulation. The present study establishes a connection between morphology and a broader natural component, climate, and introduces new questions about the spatial distribution of morphological variation among squamates.