Ecological responses of squamate reptiles to nocturnal warming.

Nocturnal temperatures are increasing at a pace exceeding diurnal temperatures in most parts of the world. The role of warmer nocturnal temperatures in animal ecology has received scant attention and most studies focus on diurnal or daily descriptors of thermal environments' temporal trends. Yet, available evidence from plant and insect studies suggests that organisms can exhibit contrasting physiological responses to diurnal and nocturnal warming. Limiting studies to diurnal trends can thus result in incomplete and misleading interpretations of the ability of species to cope with global warming. Although they are expected to be impacted by warmer nocturnal temperatures, insufficient data are available regarding the night-time ecology of vertebrate ectotherms. Here, we illustrate the complex effects of nocturnal warming on squamate reptiles, a keystone group of vertebrate ectotherms. Our review includes discussion of diurnal and nocturnal ectotherms, but we mainly focus on diurnal species for which nocturnal warming affects a period dedicated to physiological recovery, and thus may perturb activity patterns and energy balance. We first summarise the physical consequences of nocturnal warming on habitats used by squamate reptiles. Second, we describe how such changes can alter the energy balance of diurnal species. We illustrate this with empirical data from the asp viper (Vipera aspis) and common wall lizard (Podarcis muralis), two diurnal species found throughout western Europe. Third, we make use of a mechanistic approach based on an energy-balance model to draw general conclusions about the effects of nocturnal temperatures. Fourth, we examine how warmer nights may affect squamates over their lifetime, with potential consequences on individual fitness and population dynamics. We review quantitative evidence for such lifetime effects using recent data derived from a range of studies on the European common lizard (Zootoca vivipara). Finally, we consider the broader eco-evolutionary ramifications of nocturnal warming and highlight several research questions that require future attention. Our work emphasises the importance of considering the joint influence of diurnal and nocturnal warming on the responses of vertebrate ectotherms to climate warming.

Sex- and state-dependent covariation of risk-averse and escape behavior in a widespread lizard.

Mounting evidence has shown that personality and behavioral syndromes have a substantial influence on interspecific interactions and individual fitness. However, the stability of covariation among multiple behavioral traits involved in antipredator responses has seldom been tested. Here, we investigate whether sex, gravidity, and parasite infestations influence the covariation between risk aversion (hiding time within a refuge) and escape response (immobility, escape distance) using a viviparous lizard, Zootoca vivipara, as a model system. Our results demonstrated a correlation between risk-averse and escape behavior at the among-individual level, but only in gravid females. We found no significant correlations in either males or neonates. A striking result was the loss of association in postparturition females. This suggests that the "risk-averse - escape" syndrome is ephemeral and only emerges in response to constraints on locomotion driven by reproductive burden. Moreover, parasites have the potential to dissociate the correlations between risk aversion and escape response in gravid females, yet the causal chain requires further examination. Overall, our findings provide evidence of differences in the association between behaviors within the lifetime of an individual and indicate that individual states, sex, and life stages can together influence the stability of behavioral syndromes.

Investigating the genetic basis of vertebrate dispersal combining RNA-seq, RAD-seq and quantitative genetics.

Although animal dispersal is known to play key roles in ecological and evolutionary processes such as colonization, population extinction and local adaptation, little is known about its genetic basis, particularly in vertebrates. Untapping the genetic basis of dispersal should deepen our understanding of how dispersal behaviour evolves, the molecular mechanisms that regulate it and link it to other phenotypic aspects in order to form the so-called dispersal syndromes. Here, we comprehensively combined quantitative genetics, genome-wide sequencing and transcriptome sequencing to investigate the genetic basis of natal dispersal in a known ecological and evolutionary model of vertebrate dispersal: the common lizard, Zootoca vivipara. Our study supports the heritability of dispersal in semi-natural populations, with less variation attributable to maternal and natal environment effects. In addition, we found an association between natal dispersal and both variation in the carbonic anhydrase (CA10) gene, and in the expression of several genes (TGFB2, SLC6A4, NOS1) involved in central nervous system functioning. These findings suggest that neurotransmitters (serotonin and nitric oxide) are involved in the regulation of dispersal and shaping dispersal syndromes. Several genes from the circadian clock (CRY2, KCTD21) were also differentially expressed between disperser and resident lizards, supporting that the circadian rhythm, known to be involved in long-distance migration in other taxa, might affect dispersal as well. Since neuronal and circadian pathways are relatively well conserved across vertebrates, our results are likely to be generalisable, and we therefore encourage future studies to further investigate the role of these pathways in shaping dispersal in vertebrates.

Lizards from warm and declining populations are born with extremely short telomeres.

Aging is the price to pay for acquiring and processing energy through cellular activity and life history productivity. Climate warming can exacerbate the inherent pace of aging, as illustrated by a faster erosion of protective telomere DNA sequences. This biomarker integrates individual pace of life and parental effects through the germline, but whether intra- and intergenerational telomere dynamics underlies population trends remains an open question. Here, we investigated the covariation between life history, telomere length (TL), and extinction risk among three age classes in a cold-adapted ectotherm (Zootoca vivipara) facing warming-induced extirpations in its distribution limits. TL followed the same threshold relationships with population extinction risk at birth, maturity, and adulthood, suggesting intergenerational accumulation of accelerated aging rate in declining populations. In dwindling populations, most neonates inherited already short telomeres, suggesting they were born physiologically old and unlikely to reach recruitment. At adulthood, TL further explained females' reproductive performance, switching from an index of individual quality in stable populations to a biomarker of reproductive costs in those close to extirpation. We compiled these results to propose the aging loop hypothesis and conceptualize how climate-driven telomere shortening in ectotherms may accumulate across generations and generate tipping points before local extirpation.

Environmental conditions and male quality traits simultaneously explain variation of multiple colour signals in male lizards.

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, carotenoid-based yellow-orange and structural UV), physiological performance, parasitism, T levels and environmental factors (microclimate, forest cover) in male common lizards Zootoca vivipara from 13 populations. We found that the three colour signals conveyed information on different aspects of male condition, supporting a multiple message hypothesis. T influenced only parasitism, suggesting that T does not directly mediate the relationships between colour signals and their information content. Moreover, colour signals became more saturated in forested habitats, suggesting an adaptation to degraded light conditions, and became generally brighter in mesic conditions, in contradiction with the thermal melanism hypothesis. We show that distinct individual quality traits and environmental factors simultaneously explain variations of multiple colour signals with different production modes. Our study therefore highlights the complexity of colour signal evolution, involving various sets of selective pressures acting at the same time, but in different ways depending on colour production mechanism.

Les lézards mâles arborent souvent plusieurs signaux colorés de nature pigmentaire et structurale qui reflètent de multiples traits de qualité (e.g. performance, parasitisme), et la testostérone (T) joue souvent un rôle de médiateur dans ces relations. En outre, les conditions environnementales peuvent également expliquer les variations des signaux colorés en influençant des aspects tels que l'efficacité des signaux, la thermorégulation ou le camouflage. Les relations entre signaux colorés, traits de qualité individuelle et facteurs environnementaux ont souvent été analysées séparément, mais rarement de manière simultanée. Ainsi, la réponse de ces multiples signaux colorés aux variations de tous ces facteurs reste à explorer dans le contexte d'une étude intégrative. Ici, nous explorons la relation entre ces multiples signaux colorés et leur contenu informatif, nous examinons le rôle de T comme médiateur potentiel de ces relations et nous recherchons si les conditions environnementales expliquent la variation de ces signaux colorés. Nous avons mené une étude intégrative afin d'examiner la covariation entre trois types de signaux colorés (noir produit par la mélanine, jaune-orange produit par les caroténoïdes et UV produit par des éléments structuraux), la performance physiologique, le parasitisme, les niveaux de T et les conditions environnementales (e.g. microclimat, couverture forestière) chez des mâles du lézard vivipare (Zootoca vivipara) provenant de 13 populations. Nos résultats indiquent que les trois signaux colorés transmettent des informations sur différents aspects de la condition des mâles, en accord avec l'hypothèse de « messages multiples ¼. T influence uniquement le parasitisme, suggérant que T n'agit pas en tant que médiateur des relations entre ces signaux colorés et leur contenu informatif. De plus, les signaux colorés sont plus saturés dans les habitats les plus forestiers, ce qui suggère une adaptation à des conditions lumineuses dégradées. Enfin, les signaux colorés sont plus intenses lorsque les conditions sont mésiques, en contradiction avec l'hypothèse du mélanisme thermal. Nous démontrons que différents traits de qualité individuelle et facteurs environnementaux expliquent de manière simultanée les variations de multiples signaux colorés impliquant différents modes de production. Notre étude souligne ainsi la complexité de l'évolution des signaux colorés, qui implique plusieurs types de pressions de sélection agissant en même temps mais dans des directions différentes selon le mode de production.

Intraspecific diversity alters the relationship between climate change and parasitism in a polymorphic ectotherm.

Climate-modulated parasitism is driven by a range of factors, yet the spatial and temporal variability of this relationship has received scant attention in wild vertebrate hosts. Moreover, most prior studies overlooked the intraspecific differences across host morphotypes, which impedes a full understanding of the climate-parasitism relationship. In the common lizard (Zootoca vivipara), females exhibit three colour morphs: yellow (Y-females), orange (O-females) and mixed (mixture of yellow and orange, M-females). Zootoca vivipara is also infested with an ectoparasite (Ophionyssus mites). We therefore used this model system to examine the intraspecific response of hosts to parasitism under climate change. We found infestation probability to differ across colour morphs at both spatial (10 sites) and temporal (20 years) scales: M-females had lower parasite infestations than Y- and O-females at lower temperatures, but became more susceptible to parasites as temperature increased. The advantage of M-females at low temperatures was counterbalanced by their higher mortality rates thereafter, which suggests a morph-dependent trade-off between resistance to parasites and host survival. Furthermore, significant interactions between colour morphs and temperature indicate that the relationship between parasite infestations and climate warming was contingent on host morphotypes. Parasite infestations increased with temperature for most morphs, but displayed morph-specific rates. Finally, infested M-females had higher reductions in survival rates than infested Y- or O-females, which implies a potential loss of intraspecific diversity within populations as parasitism and temperatures rise. Overall, we found parasitism increases with warming temperatures, but this relationship is modulated by host morphotypes and an interaction with temperature. We suggest that epidemiological models incorporate intraspecific diversity within species for better understanding the dynamics of wildlife diseases under climate warming.

Intense nocturnal warming alters growth strategies, colouration and parasite load in a diurnal lizard.

In the past decades, nocturnal temperatures have been playing a disproportionate role in the global warming of the planet. Yet, they remain a neglected factor in studies assessing the impact of global warming on natural populations. Here, we question whether an intense augmentation of nocturnal temperatures is beneficial or deleterious to ectotherms. Physiological performance is influenced by thermal conditions in ectotherms and an increase in temperature by only 2°C is sufficient to induce a disproportionate increase in metabolic expenditure. Warmer nights may expand ectotherms' species thermal niche and open new opportunities for prolonged activities and improve foraging efficiency. However, increased activity may also have deleterious effects on energy balance if exposure to warmer nights reduces resting periods and elevates resting metabolic rate. We assessed whether warmer nights affected an individual's growth, dorsal skin colouration, thermoregulation behaviour, oxidative stress status and parasite load by exposing yearling common lizards (Zootoca vivipara) from four populations to either ambient or high nocturnal temperatures for approximately 5 weeks. Warmer nocturnal temperatures increased the prevalence of ectoparasitic infestation and altered allocation of resources towards structural growth rather than storage. We found no change in markers for oxidative stress. The thermal treatment did not influence thermal preferences, but influenced dorsal skin brightness and luminance, in line with a predicted acclimation response in colder environments to enhance heat gain from solar radiation. Altogether, our results highlight the importance of considering nocturnal warming as an independent factor affecting ectotherms' life history in the context of global climate change. ​.

Climate dependent heating efficiency in the common lizard.

Regulation of body temperature is crucial for optimizing physiological performance in ectotherms but imposes constraints in time and energy. Time and energy spent thermoregulating can be reduced through behavioral (e.g., basking adjustments) or biophysical (e.g., heating rate physiology) means. In a heterogeneous environment, we expect thermoregulation costs to vary according to local, climatic conditions and therefore to drive the evolution of both behavioral and biophysical thermoregulation. To date, there are limited data showing that thermal physiological adjustments have a direct relationship to climatic conditions. In this study, we explored the effect of environmental conditions on heating rates in the common lizard (Zootoca vivipara). We sampled lizards from 10 populations in the Massif Central Mountain range of France and measured whether differences in heating rates of individuals correlated with phenotypic traits (i.e., body condition and dorsal darkness) or abiotic factors (temperature and rainfall). Our results show that heat gain is faster for lizards with a higher body condition, but also for individuals from habitats with higher amount of precipitation. Altogether, they demonstrate that environmentally induced constraints can shape biophysical aspects of thermoregulation.

High-elevation hypoxia impacts perinatal physiology and performance in a potential montane colonizer.

Climate change is generating range shifts in many organisms, notably along the elevational gradient in mountainous environments. However, moving up in elevation exposes organisms to lower oxygen availability, which may reduce the successful reproduction and development of oviparous organisms. To test this possibility in an upward-colonizing species, we artificially incubated developing embryos of the viperine snake (Natrix maura) using a split-clutch design, in conditions of extreme high elevation (hypoxia at 2877 m above sea level; 72% sea-level equivalent O2 availability) or low elevation (control group; i.e. normoxia at 436 m above sea level). Hatching success did not differ between the two treatments. Embryos developing at extreme high elevation had higher heart rates and hatched earlier, resulting in hatchlings that were smaller in body size and slower swimmers compared to their siblings incubated at lower elevation. Furthermore, post-hatching reciprocal transplant of juveniles showed that snakes which developed at extreme high elevation, when transferred back to low elevation, did not recover full performance compared to their siblings from the low elevation incubation treatment. These results suggest that incubation at extreme high elevation, including the effects of hypoxia, will not prevent oviparous ectotherms from producing viable young, but may pose significant physiological challenges on developing offspring in ovo. These early-life performance limitations imposed by extreme high elevation could have negative consequences on adult phenotypes, including on fitness-related traits.

The interplay between movement, morphology and dispersal in Tetrahymena ciliates.

Understanding how and why individual movement translates into dispersal between populations is a long-term goal in ecology. Movement is broadly defined as 'any change in the spatial location of an individual', whereas dispersal is more narrowly defined as a movement that may lead to gene flow. Because the former may create the condition for the latter, behavioural decisions that lead to dispersal may be detectable in underlying movement behaviour. In addition, dispersing individuals also have specific sets of morphological and behavioural traits that help them coping with the costs of movement and dispersal, and traits that mitigate costs should be under selection and evolve if they have a genetic basis. Here, we experimentally study the relationships between movement behaviour, morphology and dispersal across 44 genotypes of the actively dispersing unicellular, aquatic model organism Tetrahymena thermophila. We used two-patch populations to quantify individual movement trajectories, as well as activity, morphology and dispersal rate. First, we studied variation in movement behaviour among and within genotypes (i.e. between dispersers and residents) and tested whether this variation can be explained by morphology. Then, we addressed how much the dispersal rate is driven by differences in the underlying movement behaviour. Genotypes revealed clear differences in terms of movement speed and linearity. We also detected marked movement differences between resident and dispersing individuals, mediated by the genotype. Movement variation was partly explained by morphological properties such as cell size and shape, with larger cells consistently showing higher movement speed and higher linearity. Genetic differences in activity and movement were positively related to the observed dispersal and jointly explained 47% of the variation in dispersal rate. Our study shows that a detailed understanding of the interplay between morphology, movement and dispersal may have potential to improve dispersal predictions over broader spatio-temporal scales.

Variability in Dispersal Syndromes Is a Key Driver of Metapopulation Dynamics in Experimental Microcosms.

Evolutionary ecology studies have increasingly focused on the impact of intraspecific variability on population processes. However, the role such variation plays in the dynamics of spatially structured populations and how it interacts with environmental changes remains unclear. Here we experimentally quantify the relative importance of intraspecific variability in dispersal-related traits and spatiotemporal variability of environmental conditions for the dynamics of two-patch metapopulations using clonal genotypes of a ciliate in connected microcosms. We demonstrate that in our simple two-patch microcosms, differences among genotypes are at least as important as spatiotemporal variability of resources for metapopulation dynamics. Furthermore, we show that an important proportion of this effect results from variability of dispersal syndromes. These syndromes can therefore be as important for metapopulation dynamics as spatiotemporal variability of environmental conditions. This study demonstrates that intraspecific variability in dispersal syndromes can be key in the functioning of metapopulations facing environmental changes.

Environmental variation mediates the prevalence and co-occurrence of parasites in the common lizard, Zootoca vivipara.

BACKGROUND: Hosts and their parasites are under reciprocal selection, leading to coevolution. However, parasites depend not only on a host, but also on the host's environment. In addition, a single host species is rarely infested by a single species of parasite and often supports multiple species (i.e., multi-infestation). Although the arms race between a parasite and its host has been well studied, few data are available on how environmental conditions may influence the process leading to multiple infestations. In this study, we examine whether: (1) environmental factors including altitude, temperature, vegetation cover, human disturbance, and grazing by livestock affect the prevalence of two types of ectoparasites, mites and ticks, on their host (the common lizard, Zootoca vivipara) and (2) competition is evident between mites and ticks. RESULTS: We found the probability of mite infestation increased with altitude and vegetation cover, but decreased with human disturbance and presence of livestock. In contrast, the probability of tick infestation was inversely associated with the same factors. Individuals with low body condition and males had higher mite loads. However, this pattern was not evident for tick loads. The results from a structural equation model revealed that mites and ticks indirectly and negatively affected each other's infestation probability through an interaction involving the environmental context. We detected a direct negative association between mites and ticks only when considering estimates of parasite load. This suggests that both mites and ticks could attach to the same host, but once they start to accumulate, only one of them takes advantage. CONCLUSION: The environment of hosts has a strong effect on infestation probabilities and parasite loads of mites and ticks. Autecological differences between mites and ticks, as indicated by their opposing patterns along environmental gradients, may explain the pattern of weak contemporary interspecific competition. Our findings emphasize the importance of including environmental factors and the natural history of each parasite species in studies of host-parasite coevolution.

When water interacts with temperature: Ecological and evolutionary implications of thermo-hydroregulation in terrestrial ectotherms.

The regulation of body temperature (thermoregulation) and of water balance (defined here as hydroregulation) are key processes underlying ecological and evolutionary responses to climate fluctuations in wild animal populations. In terrestrial (or semiterrestrial) ectotherms, thermoregulation and hydroregulation closely interact and combined temperature and water constraints should directly influence individual performances. Although comparative physiologists traditionally investigate jointly water and temperature regulation, the ecological and evolutionary implications of these coupled processes have so far mostly been studied independently. Here, we revisit the concept of thermo-hydroregulation to address the functional integration of body temperature and water balance regulation in terrestrial ectotherms. We demonstrate how thermo-hydroregulation provides a framework to investigate functional adaptations to joint environmental variation in temperature and water availability, and potential physiological and/or behavioral conflicts between thermoregulation and hydroregulation. We extend the classical cost-benefit model of thermoregulation in ectotherms to highlight the adaptive evolution of optimal thermo-hydroregulation strategies. Critical gaps in the parameterization of this conceptual optimality model and guidelines for future empirical research are discussed. We show that studies of thermo-hydroregulation refine our mechanistic understanding of physiological and behavioral plasticity, and of the fundamental niche of the species. This is illustrated with relevant and recent examples of space use and dispersal, resource-based trade-offs, and life-history tactics in insects, amphibians, and nonavian reptiles.

Kin-dependent dispersal influences relatedness and genetic structuring in a lek system.

Kin selection and dispersal play a critical role in the evolution of cooperative breeding systems. Limited dispersal increases relatedness in spatially structured populations (population viscosity), with the result that neighbours tend to be genealogical relatives. Yet the increase in neighbours' fitness-related performance through altruistic interaction may also result in habitat saturation and thus exacerbate local competition between kin. Our goal was to detect the footprint of kin selection and competition by examining the spatial structure of relatedness and by comparing non-effective and effective dispersal in a population of a lekking bird, Tetrao urogallus. For this purpose, we analysed capture-recapture and genetic data collected over a 6-year period on a spatially structured population of T. urogallus in France. Our findings revealed a strong spatial structure of relatedness in males. They also indicated that the population viscosity could allow male cooperation through two non-exclusive mechanisms. First, at their first lek attendance, males aggregate in a lek composed of relatives. Second, the distance corresponding to non-effective dispersal dramatically outweighed effective dispersal distance, which suggests that dispersers incur high post-settlement costs. These two mechanisms result in strong population genetic structuring in males. In females, our findings revealed a lower level of spatial structure of relatedness and genetic structure in respect to males. Additionally, non-effective dispersal and effective dispersal distances in females were highly similar, which suggests limited post-settlement costs. These results indicate that kin-dependent dispersal decisions and costs have a genetic footprint in wild populations and are factors that may be involved in the evolution of cooperative courtship.

Adaptive responses of animals to climate change are most likely insufficient.

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.

Correction: Seasonal and interpopulational phenotypic variation in morphology and sexual signals of Podarcis liolepis lizards.

[This corrects the article DOI: 10.1371/journal.pone.0211686.].

Seasonal and interpopulational phenotypic variation in morphology and sexual signals of Podarcis liolepis lizards.

Widespread species often show extensive phenotypic variation due to the contrasting abiotic and biotic factors that shape selective pressures in different environments. In this context, the gradual and predictable patterns of variation in climatic and environmental conditions found in mountain areas offer a great opportunity to explore intraspecific phenotypic variation. For instance, temperature is negatively correlated with altitude and virtually all aspects of the behavior and physiology of ectotherms are sensitive to body temperature. In this work, we tested the hypothesis that morphology, dorsal and ventral coloration and the chemical profile of femoral secretions show interpopulational and seasonal variation in the lacertid lizard (Podarcis liolepis). We compared lizards from three populations inhabiting lowland and highland habitats in the French Pyrenees that were closely related genetically. We found that highland lizards were larger, stockier, had longer heads and more femoral pores and had a darker dorsal coloration than lowland ones. In addition, we detected interpopulational differences in both the abundance and the richness of chemical compounds in the glandular secretions, and we also found seasonal variation in the overall chemical composition. Dorsal and ventral coloration differed seasonally and between populations. Ventral and dorsal brightness were higher in lowland than in highland lizards in the reproductive season whereas the reversed trend was found in the non-reproductive season but only for dorsal brightness. In addition, all lizards had browner dorsal coloration in the non-reproductive season, and lowland lizards were greener in the reproductive season. By integrating information from both visual and chemical systems, our works offers a comprehensive view of how these lizards communicate in a multimodal context.

BMC ecology image competition 2018: the winning images.

The sixth BMC Ecology Image Competition received more than 145 photographs from talented ecologists around the world, showcasing the amazing biodiversity, natural beauty and biological interactions found in nature. In this editorial, we showcase the winning images, as selected by our guest judge, Professor Zhigang Jiang from the Institute of Zoology of the Chinese Academy of Sciences, with help from the journal's editorial board. Enjoy!

Habitat choice meets thermal specialization: Competition with specialists may drive suboptimal habitat preferences in generalists.

Limited dispersal is classically considered as a prerequisite for ecological specialization to evolve, such that generalists are expected to show greater dispersal propensity compared with specialists. However, when individuals choose habitats that maximize their performance instead of dispersing randomly, theory predicts dispersal with habitat choice to evolve in specialists, while generalists should disperse more randomly. We tested whether habitat choice is associated with thermal niche specialization using microcosms of the ciliate Tetrahymena thermophila, a species that performs active dispersal. We found that thermal specialists preferred optimal habitats as predicted by theory, a link that should make specialists more likely to track suitable conditions under environmental changes than expected under the random dispersal assumption. Surprisingly, generalists also performed habitat choice but with a preference for suboptimal habitats. Since this result challenges current theory, we developed a metapopulation model to understand under which circumstances such a preference for suboptimal habitats should evolve. We showed that competition between generalists and specialists may favor a preference for niche margins in generalists under environmental variability. Our results demonstrate that the behavioral dimension of dispersal-here, habitat choice-fundamentally alters our predictions of how dispersal evolve with niche specialization, making dispersal behaviors crucial for ecological forecasting facing environmental changes.

Species dispersal and biodiversity in human-dominated metacommunities.

The concept of the Anthropocene is based on the idea that human impacts are now the primary drivers of changes in the earth's systems, including ecological systems. In many cases, the behavior that causes ecosystem change is itself triggered by ecological factors. Yet most ecological models still treat human impacts as given, and frequently as constant. This undermines our ability to understand the feedbacks between human behavior and ecosystem change. Focusing on the problem of species dispersal, we evaluate the effect of dispersal on biodiversity in a system subject to predation by humans. People are assumed to obtain benefits from (a) the direct consumption of species (provisioning services), (b) the non-consumptive use of species (cultural services), and (c) the buffering effects of the mix of species (regulating services). We find that the effects of dispersal on biodiversity depend jointly on the competitive interactions among species, and on human preferences over species and the services they provide. We find that while biodiversity may be greatest at intermediate levels of dispersal, this depends on structure of preferences across the metacommunity.