Variation in the risk of predation may profoundly affect the evolution of anti-predator behaviour... more Variation in the risk of predation may profoundly affect the evolution of anti-predator behaviours. Theory predicts that selection would favour enhanced locomotor capacity in highrisk environments, such as open habitats. An earlier study demonstrated significant intrapopulation and intersexual variation in wariness and sprint speed among the lava lizards (Microlophus albemarlensis) that was concordant with presumed risk of predation on Isla Plaza Sur in the Galápagos Archipelago. In particular, males and females from sparsely vegetated areas had greater approach and flight distances than those of more highly vegetated areas; males were also faster than females. We now compare endurance capacities of males and females from the same population on Isla Plaza Sur. We predicted the higher presumed risk of predation in the sparsely vegetated region would favour enhanced performance capacities. In addition, we predicted that sexual selection for territory defence would favour males that had the ability to flee long distances. Lizards from the sparsely vegetated area did have higher endurance than those from the vegetated area. Males had higher endurance times than females, but this difference was an outcome of body size, which was inconsistent with the sexual selection hypothesis. The significant differences in endurance between locations combined with the absence of dimorphism in performance suggest that the intrapopulation differences are an outcome of natural selection for predator escape.
We describe new ESS models of density regulation driven by genic selection to explain the cyclica... more We describe new ESS models of density regulation driven by genic selection to explain the cyclical dynamics of a social system that exhibits a rock-paper-scissors (RPS) set of three alternative strategies. We tracked changes in morph frequency and fitness of Lacerta vivipara and found conspicuous RPS cycles. Morphs of Uta and Lacerta exhibited parallel survival-performance trade-offs. Frequency cycles in both species of lizards are driven by genic selection. In Lacerta, frequency of each allele in adult cohorts had significant impacts on juvenile recruitment, similar to mutualistic, altruistic, and antagonistic relations of RPS alleles in Uta. We constructed evolutionarily stable strategy (ESS) models in which adults impact juvenile recruitment as a function of self versus nonself color rec-
Mating system theory based on economics of resource defense has been applied to describe social s... more Mating system theory based on economics of resource defense has been applied to describe social system diversity across taxa. Such models are generally successful but fail to account for stable mating systems across different environments or shifts in mating system without a change in ecological conditions. We propose an alternative approach to resource defense theory based on frequencydependent competition among genetically determined alternative behavioral strategies characterizing many social systems (polygyny, monogamy, sneak). We modeled payoffs for competition, neighborhood choice, and paternal care to determine evolutionary transitions among mating systems. Our model predicts four stable outcomes driven by the balance between cooperative and agonistic behaviors: promiscuity (two or three strategies), polygyny, and monogamy. Phylogenetic analysis of 288 rodent species supports assumptions of our model and is consistent with patterns of evolutionarily stable states and mating system transitions. Support for model assumptions include that monogamy and polygyny evolve from promiscuity and that paternal care and monogamy are coadapted in rodents. As predicted by our model, monogamy and polygyny occur in sister taxa among rodents more often than by chance. Transitions to monogamy also favor higher speciation rates in subsequent lineages, relative to polygynous sister lineages. Taken together, our results suggest that genetically based neighborhood choice behavior and paternal care can drive transitions in mating system evolution. While our genic mating system theory could complement resource-based theory, it can explain mating system transitions regardless of resource distribution and provides alternative explanations, such as evolutionary inertia, when resource ecology and mating systems do not match.
General and Comparative Endocrinology, Mar 1, 2017
Arginine vasotocin (AVT) is known to play an important role in the regulation of social behavior ... more Arginine vasotocin (AVT) is known to play an important role in the regulation of social behavior in a number of vertebrate species. Nevertheless, the relationship between AVT and intraspecific interactions appears complex and in some cases contradictory. Moreover, AVT influences other behaviors, which are not primarily social including exploratory behavior, locomotion and thermoregulation. Some of these behavioral effects may be side-effects from a general influence of AVT on physiology. Indeed AVT can regulate metabolism and osmoregulation. Because most studies have been conducted using mammals and birds, its role in modulating behavior in other vertebrate groups is largely unknown. In this study we examined the effect of AVT on the social behavior of male common lizards, Zootoca vivipara. Moreover, considering the variety of pathways AVT could be involved in, we investigated its consequences on thermoregulatory behavior and physiological performance. In mid-June 2010, 74 males were captured from field sites (Mont-Lozère, South-eastern France) and kept in the laboratory for three weeks to obtain behavioral (reaction to conspecific odors, thermoregulation) and physiological (endurance, testosterone level) measurements. We demonstrated that injection of AVT reduced testosterone level and affected social behavior in different ways depending on the size of an individual. Specifically, small males injected with AVT were less attracted by conspecific odors than small control males, and no effect was detected in large males. Moreover, AVT promoted thermoregulatory behavior and enhanced endurance. These results are concordant with previous results obtained in this species in studies on stress suggesting that AVT may act through its influence on corticosterone secretion.
Proceedings of The Royal Society B: Biological Sciences, May 9, 2018
Ectothermic species are particularly sensitive to changes in temperature and may adapt to changes... more Ectothermic species are particularly sensitive to changes in temperature and may adapt to changes in thermal environments through evolutionary shifts in thermal physiology or thermoregulatory behaviour. Nevertheless, the heritability of thermal traits, which sets a limit on evolutionary potential, remains largely unexplored. In this study, we captured brown anole lizards (Anolis sagrei) from two populations that occur in contrasting thermal environments. We raised offspring from these populations in a laboratory common garden and compared the shape of their thermal performance curves to test for genetic divergence in thermal physiology. Thermal performance curves differed between populations in a common garden in ways partially consistent with divergent patterns of natural selection experienced by the source populations, implying that they had evolved in response to selection. Next, we estimated the heritability of thermal performance curves and of several traits related to thermoregulatory behaviour. We did not detect significant heritability in most components of the thermal performance curve or in several aspects of thermoregulatory behaviour, suggesting that contemporary selection is unlikely to result in rapid evolution. Our results indicate that the response to selection may be slow in the brown anole and that evolutionary change is unlikely to keep pace with current rates of environmental change.
Male lizards often display multiple pigment‐based and structural colour signals which may reflect... more Male lizards often display multiple pigment‐based and structural colour signals which may reflect various quality traits (e.g. performance, parasitism), with testosterone (T) often mediating these relationships. Furthermore, environmental conditions can explain colour signal variation by affecting processes such as signal efficacy, thermoregulation and camouflage. The relationships between colour signals, male quality traits and environmental factors have often been analysed in isolation, but simultaneous analyses are rare. Thus, the response of multiple colour signals to variation in all these factors in an integrative analysis remains to be investigated. Here, we investigated how multiple colour signals relate to their information content, examined the role of T as a potential mediator of these relationships and how environmental factors explain colour signal variation. We performed an integrative study to examine the covariation between three colour signals (melanin‐based black, ...
Climate change is one of the most pressing challenges for ectotherms due to their dependence on e... more Climate change is one of the most pressing challenges for ectotherms due to their dependence on environmental temperature. Extirpation of populations of lizards have already been reported, including endemic species occurring in the mountains of Central México. Here, we characterize the thermal ecology of a montane, viviparous lizard species, Barisia imbricata. In addition, we use thermal and physiological traits to predict the persistence of the species in face of climate change. We collected individuals from two populations at its lower and upper elevational limits, recorded eld body temperature (T b ), operative environmental temperatures (T e ), preferred body temperature (T pref ) and the thermal sensitivity of endurance. We calculated the hours of activity (h a ) and hours of restriction (h r ) using a mechanistic-ecophysiological model. We then applied a species distribution model that integrates core ecophysiological traits (T b , T pref , thermal performance breadth, optimal temperature for performance, critical thermal maximum and minimum) with climate variables to determine potential shifts in habitat occupancy. Finally, we used a mechanistic niche model that includes estimates of h r and h a to predict the probability of persistence of the species under three scenarios of climate change between now and by 2070. We found that B. imbricata has a broad performance breadth, which suggests it is a thermal generalist, and is capable of activity across a broad range of T e . The mechanisticecophysiological niche model predicts that B. imbricata faces serious distributional restrictions at low elevations, but populations at higher elevations should persist if the habitat remains intact.
Behavioral thermoregulation is an efficient mechanism to buffer the physiological effects of clim... more Behavioral thermoregulation is an efficient mechanism to buffer the physiological effects of climate change. Thermal ecology studies have traditionally tested how thermal constraints shape thermoregulatory behaviors without accounting for the potential major effects of landscape structure and water availability. Thus, we lack a general understanding of the multifactorial determinants of thermoregulatory behaviors in natural populations. In this study, we quantified the relative contribution of elevation, thermal gradient, moisture gradient, and landscape structure in explaining geographic variation in thermoregulation strategies of a terrestrial ectotherm species. We measured field‐active body temperature, thermal preferences, and operative environmental temperatures to calculate thermoregulation indices, including thermal quality of the habitat and thermoregulation efficiency for a very large sample of common lizards (Zootoca vivipara) from 21 populations over 3 yr across the Massi...
Caudal autotomy is a striking adaptation used by many lizard species to evade predators. Most stu... more Caudal autotomy is a striking adaptation used by many lizard species to evade predators. Most studies to date indicate that caudal autotomy impairs lizard locomotor performance. Surprisingly, some species bearing the longest tails show negligible impacts of caudal autotomy on sprint speed. Part of this variation has been attributed to lineage effects. For the first time, we model the effects of caudal autotomy on the locomotor performance of a gymnophthalmid lizard, Micrablepharus atticolus, which has a long and bright blue tail. To improve model accuracy, we incorporated the effects of several covariates. We found that body temperature, pregnancy, mass, collection site, and the length of the regenerated portion of the tail were the most important predictors of locomotor performance. However, sprint speed was unaffected by tail loss. Apparently, the long tail of M. atticolus is more useful when using undulation amidst the leaf litter and not when using quadrupedal locomotion on a fl...
Mating system theory based on economics of resource defense has been applied to describe social s... more Mating system theory based on economics of resource defense has been applied to describe social system diversity across taxa. Such models are generally successful but fail to account for stable mating systems across different environments or shifts in mating system without a change in ecological conditions. We propose an alternative approach to resource defense theory based on frequencydependent competition among genetically determined alternative behavioral strategies characterizing many social systems (polygyny, monogamy, sneak). We modeled payoffs for competition, neighborhood choice, and paternal care to determine evolutionary transitions among mating systems. Our model predicts four stable outcomes driven by the balance between cooperative and agonistic behaviors: promiscuity (two or three strategies), polygyny, and monogamy. Phylogenetic analysis of 288 rodent species supports assumptions of our model and is consistent with patterns of evolutionarily stable states and mating system transitions. Support for model assumptions include that monogamy and polygyny evolve from promiscuity and that paternal care and monogamy are coadapted in rodents. As predicted by our model, monogamy and polygyny occur in sister taxa among rodents more often than by chance. Transitions to monogamy also favor higher speciation rates in subsequent lineages, relative to polygynous sister lineages. Taken together, our results suggest that genetically based neighborhood choice behavior and paternal care can drive transitions in mating system evolution. While our genic mating system theory could complement resource-based theory, it can explain mating system transitions regardless of resource distribution and provides alternative explanations, such as evolutionary inertia, when resource ecology and mating systems do not match.
Climatic conditions changing over time and space shape the evolution of organisms at multiple lev... more Climatic conditions changing over time and space shape the evolution of organisms at multiple levels, including temperate lizards in the family Lacertidae. Here we reconstruct a dated phylogenetic tree of 262 lacertid species based on a supermatrix relying on novel phylogenomic datasets and fossil calibrations. Diversification of lacertids was accompanied by an increasing disparity among occupied bioclimatic niches, especially in the last 10 Ma, during a period of progressive global cooling. Temperate species also underwent a genome-wide slowdown in molecular substitution rates compared to tropical and desert-adapted lacertids. Evaporative water loss and preferred temperature are correlated with bioclimatic parameters, indicating physiological adaptations to climate. Tropical, but also some populations of cool-adapted species experience maximum temperatures close to their preferred temperatures. We hypothesize these species-specific physiological preferences may constitute a handica...
Covariation among behavioral and physiological traits is thought to enhance reproductive success ... more Covariation among behavioral and physiological traits is thought to enhance reproductive success and Darwinian fitness. Species that exhibit alternative mating strategies provide excellent opportunities to assess the relative contributions of physiological and behavioral traits to fitness. Male side-blotched lizards (Uta stansburiana) exhibit three heritable throat color morphs that are associated with alternative mating behaviors. The three morphs differ in resource holding potential, mate attraction, mate defense, and physiological performance. We examined interrelationships of body mass, stamina, field metabolic rate, growth rate, and survival to the second capture (a fitness proxy). Relationships among variables were complex, and mass, stamina, and throat color interacted to predict male survival. Our analyses suggest that male side-blotched lizards exhibit trade-offs among physiological traits related to reproductive success and survival and that differential survival for different combinations of traits has caused correlational selection, leading to adaptive integration of phenotypic traits associated with alternative mating strategies.
Knowledge of the thermal ecology of a species can improve model predictions for temperatureinduce... more Knowledge of the thermal ecology of a species can improve model predictions for temperatureinduced population collapse, which in light of climate change is increasingly important for species with limited distributions. Here, we use a multi-faceted approach to quantify and integrate the thermal ecology, properties of the thermal habitat, and past and present distribution of the diurnal, xeric-adapted, and active-foraging Namibian lizard Pedioplanis husabensis (Sauria: Lacertidae) to model its local extinction risk under future climate change scenarios. We asked whether climatic conditions in various regions of its range are already so extreme that local extirpations of P. husabensis have already occurred, or whether this micro-endemic species is adapted to these extreme conditions and uses behavior to mitigate the environmental challenges. To address this, we collected thermoregulation and climate data at a micro-scale level and combined it with micro-and macroclimate data across the species' range to model extinction risk. We found that P. husabensis inhabits a thermally harsh environment, but also has high thermal preference. In cooler parts of its range, individuals are capable of leaving thermally favorable conditions-based on the species' thermal preference-unused during the day, probably to maintain low metabolic rates. Furthermore, during the summer, we observed that individuals regulate at body temperatures below the species' high thermal preference to avoid body temperatures approaching the critical thermal maximum. We find that populations of this species are currently persisting even at the hottest localities within the species' geographic distribution. We found no evidence of range shifts since the 1960s despite a documented increase in air temperatures. Nevertheless, P. husabensis only has a small safety margin between the upper limit of its thermal preference and the critical thermal maximum and might undergo range reductions in the near future under even the most moderate climate change scenarios.
Proceedings of the Royal Society B: Biological Sciences, 2018
Ectothermic species are particularly sensitive to changes in temperature and may adapt to changes... more Ectothermic species are particularly sensitive to changes in temperature and may adapt to changes in thermal environments through evolutionary shifts in thermal physiology or thermoregulatory behaviour. Nevertheless, the heritability of thermal traits, which sets a limit on evolutionary potential, remains largely unexplored. In this study, we captured brown anole lizards ( Anolis sagrei ) from two populations that occur in contrasting thermal environments. We raised offspring from these populations in a laboratory common garden and compared the shape of their thermal performance curves to test for genetic divergence in thermal physiology. Thermal performance curves differed between populations in a common garden in ways partially consistent with divergent patterns of natural selection experienced by the source populations, implying that they had evolved in response to selection. Next, we estimated the heritability of thermal performance curves and of several traits related to thermo...
1.Climate change should lead to massive loss of biodiversity in most taxa but the detailed physio... more 1.Climate change should lead to massive loss of biodiversity in most taxa but the detailed physiological mechanisms underlying population extinction remain largely elusive so far. In vertebrates, baseline levels of hormones such as glucocorticoids (GCs) may be indicators of population state since their secretion to chronic stress can impair survival and reproduction. However, the relationship between GC secretion, climate change and population extinction risk remains unclear. 2.In this study we investigated whether levels of baseline corticosterone (the main GCs in reptiles) correlate with environmental conditions and associated extinction risk across wild populations of the common lizard Zootoca vivipara. 3.First, we performed a cross-sectional comparison of baseline corticosterone levels along an altitudinal gradient among 14 populations. Then, we used a longitudinal study in 8 populations to examine the changes in corticosterone levels following the exposure to a heat wave period...
We summarize thermal-biology data of 69 species of Amazonian lizards, including mode of thermoreg... more We summarize thermal-biology data of 69 species of Amazonian lizards, including mode of thermoregulation and field-active body temperatures (Tb). We also provide new data on preferred temperatures (Tpref), voluntary and thermal-tolerance ranges, and thermal-performance curves (TPC's) for 27 species from nine sites in the Brazilian Amazonia. We tested for phylogenetic signal and pairwise correlations among thermal traits. We found that species generally categorized as thermoregulators have the highest mean values for all thermal traits, and broader ranges for Tb, critical thermal maximum (CTmax) and optimal (Topt) temperatures. Species generally categorized as thermoconformers have large ranges for Tpref, critical thermal minimum (CTmin), and minimum voluntary (VTmin) temperatures for performance. Despite these differences, our results show that all thermal characteristics overlap between both groups and suggest that Amazonian lizards do not fit into discrete thermoregulatory cat...
Temperature increases can impact biodiversity and predicting their effects is one of the main cha... more Temperature increases can impact biodiversity and predicting their effects is one of the main challenges facing global climate-change research. Ectotherms are sensitive to temperature change and, although predictions indicate that tropical species are highly vulnerable to global warming, they remain one of the least studied groups with respect to the extent of physiological variation and local extinction risks. We model the extinction risks for a tropical heliothermic teiid lizard (Kentropyx calcarata) integrating previously obtained information on intraspecific phylogeographic structure, eco-physiological traits and contemporary species distributions in the Amazon rainforest and its ecotone to the Cerrado savannah. We also investigated how thermal-biology traits vary throughout the species' geographic range and the consequences of such variation for lineage vulnerability. We show substantial variation in thermal tolerance of individuals among thermally distinct sites. Thermal c...
Proceedings of the Royal Society B: Biological Sciences, 2017
Climate change is resulting in a radical transformation of the thermal quality of habitats across... more Climate change is resulting in a radical transformation of the thermal quality of habitats across the globe. Whereas species have altered their distributions to cope with changing environments, the evidence for adaptation in response to rising temperatures is limited. However, to determine the potential of adaptation in response to thermal variation, we need estimates of the magnitude and direction of natural selection on traits that are assumed to increase persistence in warmer environments. Most inferences regarding physiological adaptation are based on interspecific analyses, and those of selection on thermal traits are scarce. Here, we estimate natural selection on major thermal traits used to assess the vulnerability of ectothermic organisms to altered thermal niches. We detected significant directional selection favouring lizards with higher thermal preferences and faster sprint performance at their optimal temperature. Our analyses also revealed correlational selection betwee...
General and comparative endocrinology, Jan 26, 2016
Arginine vasotocin (AVT) is known to play an important role in the regulation of social behavior ... more Arginine vasotocin (AVT) is known to play an important role in the regulation of social behavior in a number of vertebrate species. Nevertheless, the relationship between AVT and intraspecific interactions appears complex and in some cases contradictory. Moreover, AVT influences other behaviors, which are not primarily social including exploratory behavior, locomotion and thermoregulation. Some of these behavioral effects may be side-effects from a general influence of AVT on physiology. Indeed AVT can regulate metabolism and osmoregulation. Because most studies have been conducted using mammals and birds, its role in modulating behavior in other vertebrate groups is largely unknown. In this study we examined the effect of AVT on the social behavior of male common lizards, Zootoca vivipara. Moreover, considering the variety of pathways AVT could be involved in, we investigated its consequences on thermoregulatory behavior and physiological performance. In mid-June 2010, 74 males wer...
Sexual size dimorphism (SSD) is often assumed to reflect the phenotypic consequences of different... more Sexual size dimorphism (SSD) is often assumed to reflect the phenotypic consequences of differential selection operating on each sex. Species that exhibit SSD may also show intersexual differences in other traits, including field-active body temperatures, preferred temperatures, and locomotor performance. For these traits, differences may be correlated with differences in body size or reflect sexspecific trait optima. Male and female Yarrow's spiny lizards, Sceloporus jarrovii, in a population in southeastern Arizona exhibit a difference in body temperature that is unrelated to variation in body size. The observed sexual variation in body temperature may reflect divergence in thermal physiology between the sexes. To test this hypothesis, we measured the preferred body temperatures of male and female lizards when recently fed and fasted. We also estimated the thermal sensitivity of stamina at seven body temperatures. Variation in these traits provided an opportunity to determine whether body size or sex-specific variation unrelated to size shaped their thermal physiology. Female lizards, but not males, preferred a lower body temperature when fasted, and this pattern was unrelated to body size. Larger individuals exhibited greater stamina, but we detected no significant effect of sex on the shape or height of the thermal performance curves. The thermal preference of males and females in a thermal gradient exceeded the optimal temperature for performance in both sexes. Our findings suggest that differences in thermal physiology are both sex-and sizebased and that peak performance at low body temperatures may be adaptive given the reproductive cycles of this viviparous species. We consider the implications of our findings for the persistence of S. jarrovii and other montane ectotherms in the face of climate warming.
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Papers by Donald Miles