Paulina Artacho

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 asperse (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, &bgr; = -0.106 ± 0.06; P = 0.001) and quadratic (stabilizing selection, &ggr; = -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.

Interindividual variation in thermal sensitivity of maximal sprint speed, thermal behavior, and resting metabolic rate in a lizard.

Studies of the relationship of performance and behavioral traits with environmental factors have tended to neglect interindividual variation even though quantification of this variation is fundamental to understanding how phenotypic traits can evolve. In ectotherms, functional integration of locomotor performance, thermal behavior, and energy metabolism is of special interest because of the potential for coadaptation among these traits. For this reason, we analyzed interindividual variation, covariation, and repeatability of the thermal sensitivity of maximal sprint speed, preferred body temperature, thermal precision, and resting metabolic rate measured in ca. 200 common lizards (Zootoca vivipara) that varied by sex, age, and body size. We found significant interindividual variation in selected body temperatures and in the thermal performance curve of maximal sprint speed for both the intercept (expected trait value at the average temperature) and the slope (measure of thermal sensitivity). Interindividual differences in maximal sprint speed across temperatures, preferred body temperature, and thermal precision were significantly repeatable. A positive relationship existed between preferred body temperature and thermal precision, implying that individuals selecting higher temperatures were more precise. The resting metabolic rate was highly variable but was not related to thermal sensitivity of maximal sprint speed or thermal behavior. Thus, locomotor performance, thermal behavior, and energy metabolism were not directly functionally linked in the common lizard.

Cyclic gas-exchange in the Chilean red cricket: inter-individual variation and thermal dependence.

SUMMARY One of the most puzzling features of respiration in insects is cyclic gas exchange (CGE, the extreme form of discontinuous gas exchange-cycles, DGC), a periodic respiratory pattern that appeared independently several times in the evolution of arthropods. Although it is a striking feature of insects and some non-insect species, to date there is no clear knowledge of how widespread it is, or its adaptive significance. Here we show for the first time that a cricket (Cratomelus armatus) from the Stenopelmatidae family exhibits CGE. C. armatus shows a conspicuous, convective O-phase, with significantly repeatable ventilatory period and O-phase duration (intraclass correlation coefficients of 0.51 and 0.74, respectively). Also, C. armatus exhibits high variation in the CGE patterns, ranging from continuous to highly periodic records, sometimes including the classic F-phase. No record went to zero and we found significant (inverse) effects of ambient temperature on O-phase duration but not on the ventilatory period. Average V̇CO2 and O-phase amplitude (i.e. mean V̇CO2 of the peaks) increased with temperature whereas the amplitude of the interburst did not change significantly with ambient temperature. C. armatus is a species that lives below ground in humid forests, so our results support the chthonic-hygric hypothesis (i.e. facilitation of gas exchange under hypoxic and hypercapnic conditions, minimizing evaporative water loss), although this assertion needs to be confirmed statistically by a strong inference approach.

Do personalities co-vary with metabolic expenditure and glucocorticoid stress response in adult lizards?

Stable differences in physiology among individuals may facilitate the evolution of consistent individual differences in behavior. In particular, according to the pace-of-life syndrome (POLS) hypothesis, individual variation in metabolic expenditure and stress physiology should be linked with exploration, aggression, or risk-taking behaviors. Previous studies have uncovered stable individual differences in metabolic expenditure and circulating glucorticoids in common lizards (Zootoca vivipara). We tested the correlations between standard metabolic rates (SMR), glucorticoid stress response, and behavioral traits (activity, aggressiveness, risk taking, and sociability) in males. In ectotherms, the thermal dependence of SMR should be included in the POLS hypothesis; we therefore measured SMR at three temperatures from rest to preferred body temperature. Activity, aggressiveness, and risk taking, but not sociability, exhibited significant, short-term repeatability, and little correlation was found between behavioral traits. The SMR of lizards with a low metabolism at rest increased faster with body temperature. The SMR at rest was negatively correlated with behavioral variation in sociability and activity but not with risk-taking behavior. In addition, the plasma corticosterone level after an acute handling stress increased slightly but not significantly with aggressiveness. We discuss alternative interpretations for these relationships and conclude that the link between inter-individual variation in physiology and behavior is trait-dependent in the common lizard.Significance statementSelection better promotes the evolution of consistent differences in behavior, or personalities, when they are coupled with differences in physiology. In adult common lizards, inter-individual differences in metabolic expenditure and glucocorticoid stress response are consistent and could play a crucial role in the maintenance of personalities. This study supported partially this hypothesis. We found that more sociable and active personality types had a lower metabolic expenditure, while more aggressive personality types tended to have a higher physiological stress response. At the same time, physiology was not correlated with individual differences in risk-taking behavior and drove little part of behavioral variation. The coupling between personalities and physiology appears to be trait-dependent, suggesting that behaviors may be relatively free to evolve independently from physiology.

Intrapopulation Variation in the Standard Metabolism of a Terrestrial Mollusc: Repeatability of the CO2 Production in the Land Snail Helix aspersa

During the past 2 decades, interest in interindividual variation in performance traits has increased considerably among physiological ecologists. A great deal of this interest has focused on repeatability studies of physiological traits. One of the most important physiological traits in animals is whole‐animal metabolism because it reflects several aspects of an organism’s energy budget. However, in order to respond to natural selection (ultimately), this variable should be consistent over most of an individual’s life history. We studied energy metabolism (CO2 production, V̇co2) in two of the southernmost populations of Helix aspersa land snails, a cosmopolitan species that colonized most of the human‐inhabited world. Our results show that H. aspersa exhibits a relatively lower than expected V̇co2 compared with that described in the few other published studies on this species and that there is no significant difference between populations (Valdivia V̇co2 = 0.21 ± 0.01 mL CO2 h−1; Concepción V̇co2 = 0.20 ± 0.01 mL CO2 h−1; mean body mass = 4.2 g). Repeatability of V̇co2 in land snails was significant and was not statistically different in both populations (Valdivia: τ = 0.42; Concepción: τ = 0.31). These results suggest that energy metabolism is repeatable and can eventually respond to selection in land snails. We argue that land snails are good, though underutilized, models for evolutionary physiology studies.

Geographic variation and acclimation effects on thermoregulation behavior in the widespread lizard Liolaemus pictus

Populations at the warm range margins of the species distribution may be at the greatest risks of extinction from global warming unless they can tolerate extreme environmental conditions. Yet, some studies suggest that the thermal behavior of some lizard species is evolutionarily rigid. During two successive years, we compared the thermal biology of two populations of Liolaemus pictus living at the northern (warmer) and one population living at the southern (colder) range limits, thus spanning an 800km latitudinal distance. Populations at the two range margins belong to two deeply divergent evolutionary clades. We quantified field body temperatures (Tb), laboratory preferred body temperatures (PBT), and used operative temperature data (Te) to calculate the effectiveness of thermoregulation (E). During one year in all populations, we further exposed half of the lizards to a cold or a hot acclimation treatment to test for plasticity in the thermal behavior. The environment at the southern range limit was characterized by cooler weather and lower Te. Despite that, females had higher Tb and both males and females had higher PBT in the southernmost population (or clade) than in the northernmost populations. Acclimation to cold conditions led to higher PBT in all populations suggesting that plastic responses to thermal conditions, instead of evolutionary history, may contribute to geographic variation. Lizards regulated moderately well their body temperature (E≈0.7): they avoided warm microhabitats in the northern range but capitalized on warm microhabitats in the southern range. We review literature data to show that Liolaemus species increase their thermoregulation efficiency in thermally challenging environments. Altogether, this indicates that habitats of low thermal quality generally select against thermoconformity in these lizards.

The role of quantitative genetic studies in animal physiological ecology

Evolutionary physiology is a new discipline with roots in comparative physiology. One major change in the emergence of this discipline was an explicit new focus on viewing organisms as the evolutionary products of natural selection. The shift in research emphasis from comparative physiology to evolutionary physiology has resulted in physiological traits becoming important elements in broad research programs of evolution and ecology. Evolutionary quantitative genetics is a theory-based biological discipline that has developed the quantitative tools to test explicit evolutionary hypotheses. The role of quantitative genetics has been paramount, in studying the microevolution of morphology, behavior and life history, but not comparative physiology. As a consequence, little basic information is known such as additive genetic variation of physiological traits and the magnitude of genetically based trade-offs (i.e., genetic correlations) with other traits. Here we explore possible causes for such gap, which we believe are related with the inconsistency of what we call physiological traits across taxonomic and organizational divisions, combined with logistical problems of pedigree‐based analyses in complex traits.