Habitat‐related variation in the plasticity of a UV‐sensitive photoreceptor over a small spatial scale in the palmate newt

Plastic phenotypes are expected to be favoured in heterogeneous environments compared with stable environments. Sensory systems are interesting to test this theory because they are costly to produce and support, and strong fitness costs are expected if they are not tuned to the local environment. Consistently, the visual system of several species changes with the conditions experienced during early development. However, there is little information on whether the amplitude of the change, that is the reaction norm, differs between visual environments. Given the rapid change of many ecosystems, especially eutrophication for aquatic habitats, it is crucial to determine down to which spatial scale, change in the reaction norm occurs. We addressed this issue by quantifying the between‐habitat variation in the expression of a UV‐sensitive opsin in a newt. In western France, this species breeds in ponds of small forest patches, where water filters out UV, and in agricultural ponds where UV transmission is variable. We raised larvae from both habitats with or without exposure to UV. Opsin expression was reduced in larvae from agricultural habitats when raised without UV, whereas it was low in larvae from forest ponds under all lighting conditions. Thus, the variation in the reaction norm of opsin expression was lower in stable filtering environments and higher in heterogeneous environments. Its variation occurred between habitats across a small spatial scale. We discuss the hypotheses for this pattern and for the maintenance of residual opsin expression in forest populations.     

The heritable basis and cost of colour plasticity in coastrange sculpins

Both genetic and plastic traits contribute to adaptation in novel environments. Phenotypic plasticity can facilitate adaptation by allowing for existence in a wider range of conditions and a faster response to environmental change than gene‐based selection. Coastrange sculpins (Cottus aleuticus) colonize new and variable streams arising in the wake of receding glaciers in south‐east Alaska, and substrate‐matching plasticity may enhance colonization success by reducing detection by visual predators. As part of a long‐term study of the fitness consequences of colour plasticity and its capacity to respond to both positive and negative selection, we investigated whether it is heritable and costly. We raised full‐sib broods of sculpins in the laboratory: one half of each brood was raised in white containers, the other half in black. After 4 months, we digitally analysed their colour and found significant but weak heritability in both baseline colour and colour plasticity. To investigate the cost of colour plasticity, we compared the growth and mortality rates of juvenile sculpins reared under constant substrate colours to those reared on substrates that changed colour frequently, and compared growth rates among sculpin that differed in their colour change ability. We found evidence of small costs of plasticity, consistent with other studies of natural populations. Evidence of heritable genetic variation for plasticity and small costs to its maintenance and expression contributes to explanations of how plasticity is variable and persistent among wild populations and underscores its ability to respond both positively and negatively to selection in variable habitats.     

Male colour variation in a eurytopic African cichlid: the role of diet and hypoxia

Species that cross strong environmental gradients are expected to face divergent selective pressures that can act on sexually‐selected traits. In the present study, we examine the role of hypoxia and carotenoid availability in driving divergence in two sexually‐selected traits, male colour and reproductive behaviour, in the African cichlid Pseudocrenilabrus multicolor victoriae. Low‐dissolved oxygen (DO) (hypoxic) environments are expected to be energetically challenging; given that male nuptial colour expression and courtship displays can be costly, we expected fish in low‐DO versus high‐DO environments to differ in these traits. First, a field survey was used to describe natural variation in male nuptial colour patterns and diet across habitats divergent in DO. Next, using wild‐caught fish from a low‐DO and high‐DO habitat, we tested for differences in reproductive behaviour. Finally, a laboratory rearing experiment was used to quantify the interaction of DO and diet (low‐ versus high‐carotenoid availability) on the expression of male colour during development. In energetically challenging low‐DO environments, fish were more red and, in high‐DO environments, fish were typically brighter and more yellow. The frequency of reproductive displays in fish of low‐DO origin was 75% lower, although this had no consequence for brooding frequency (i.e. both populations produced the same number of broods on average). Our laboratory rearing study showed carotenoid availability to be important in colour production with no direct influence of DO on colour. Additionally, weak patterns of diet variation across wild populations suggest that other factors in combination with diet are contributing to colour divergence.     

Genotypic variation in phenological plasticity: Reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost

Species faced with rapidly shifting environments must be able to move, adapt, or acclimate in order to survive. One mechanism to meet this challenge is phenotypic plasticity: altering phenotype in response to environmental change. Here, we investigated the magnitude, direction, and consequences of changes in two key phenology traits (fall bud set and spring bud flush) in a widespread riparian tree species, Populus fremontii. Using replicated genotypes from 16 populations from throughout the species’ thermal range, and reciprocal common gardens at hot, warm, and cool sites, we identified four major findings: (a) There are significant genetic (G), environmental (E), and GxE components of variation for both traits across three common gardens; (b) The magnitude of phenotypic plasticity is correlated with provenance climate, where trees from hotter, southern populations exhibited up to four times greater plasticity compared to the northern, frost‐adapted populations; (c) Phenological mismatches are correlated with higher mortality as the transfer distances between provenance and garden increase; and (d) The relationship between plasticity and survival depends not only on the magnitude and direction of environmental transfer, but also on the type of environmental stress (i.e., heat or freezing), and how particular traits have evolved in response to that stress. Trees transferred to warmer climates generally showed small to moderate shifts in an adaptive direction, a hopeful result for climate change. Trees experiencing cooler climates exhibited large, non‐adaptive changes, suggesting smaller transfer distances for assisted migration. This study is especially important as it deconstructs trait responses to environmental cues that are rapidly changing (e.g., temperature and spring onset) and those that are fixed (photoperiod), and that vary across the species’ range. Understanding the magnitude and adaptive nature of phenotypic plasticity of multiple traits responding to multiple environmental cues is key to guiding restoration management decisions as climate continues to change.     

Stressful environments induce novel phenotypic variation: hierarchical reaction norms for sperm performance of a pervasive invader

Genetic variation for phenotypic plasticity is ubiquitous and important. However, the scale of such variation including the relative variability present in reaction norms among different hierarchies of biological organization (e.g., individuals, populations, and closely related species) is unknown. Complicating interpretation is a trade‐off in environmental scale. As plasticity can only be inferred over the range of environments tested, experiments focusing on fine tuned responses to normal or benign conditions may miss cryptic phenotypic variation expressed under novel or stressful environments. Here, we sought to discern the presence and shape of plasticity in the performance of brown trout sperm as a function of optimal to extremely stressful river pH, and demarcate if the reaction norm varies among genotypes. Our overarching goal was to determine if deteriorating environmental quality increases expressed variation among individuals. A more applied aim was to ascertain whether maintaining sperm performance over a wide pH range could help explain how brown trout are able to invade diverse river systems when transplanted outside of their native range. Individuals differed in their reaction norms of phenotypic expression of an important trait in response to environmental change. Cryptic variation was revealed under stressful conditions, evidenced through increasing among‐individual variability. Importantly, data on population averages masked this variability in plasticity. In addition, canalized reaction norms in sperm swimming velocities of many individuals over a very large range in water chemistry may help explain why brown trout are able to colonize a wide variety of habitats.     

Calling behaviour under climate change: geographical and seasonal variation of calling temperatures in ectotherms

Calling behaviour is strongly temperature‐dependent and critical for sexual selection and reproduction in a variety of ectothermic taxa, including anuran amphibians, which are the most globally threatened vertebrates. However, few studies have explored how species respond to distinct thermal environments at time of displaying calling behaviour, and thus it is still unknown whether ongoing climate change might compromise the performance of calling activity in ectotherms. Here, we used new audio‐trapping techniques (automated sound recording and detection systems) between 2006 and 2009 to examine annual calling temperatures of five temperate anurans and their patterns of geographical and seasonal variation at the thermal extremes of species ranges, providing insights into the thermal breadths of calling activity of species, and the mechanisms that enable ectotherms to adjust to changing thermal environments. All species showed wide thermal breadths during calling behaviour (above 15 °C) and increases in calling temperatures in extremely warm populations and seasons. Thereby, calling temperatures differed both geographically and seasonally, both in terrestrial and aquatic species, and were 8–22 °C below the specific upper critical thermal limits (CT_max) and strongly associated with the potential temperatures of each thermal environment (operative temperatures during the potential period of breeding). This suggests that calling behaviour in ectotherms may take place at population‐specific thermal ranges, diverging when species are subjected to distinct thermal environments, and might imply plasticity of thermal adjustment mechanisms (seasonal and developmental acclimation) that supply species with means of coping with climate change. Furthermore, the thermal thresholds of calling at the onset of the breeding season were dissimilar between conspecific populations, suggesting that other factors besides temperature are needed to trigger the onset of reproduction. Our findings imply that global warming would not directly inhibit calling behaviour in the study species, although might affect other temperature‐dependent features of their acoustic communication system.     

Phenotypic plasticity closely linked to climate at origin and resulting in increased mortality under warming and frost stress in a common grass

Phenotypic plasticity is important for species responses to global change and species coexistence. Phenotypic plasticity differs among species and traits and changes across environments. Here, we investigated phenotypic plasticity of the widespread grass Arrhenatherum elatius in response to winter warming and frost stress by comparing phenotypic plasticity of 11 geographically and environmentally distinct populations of this species to phenotypic plasticity of populations of different species originating from a single environment. The variation in phenotypic plasticity was similar for populations of a single species from different locations compared to populations of functionally and taxonomically diverse species from one environment for the studied traits (leaf biomass production and root integrity after frost) across three indices of phenotypic plasticity (RDPI, PIN, slope of reaction norm). Phenotypic plasticity was not associated with neutral genetic diversity but closely linked to the climate of the populations’ origin. Populations originating from warmer and more variable climates showed higher phenotypic plasticity. This indicates that phenotypic plasticity can itself be considered as a trait subject to local adaptation to climate. Finally, our data emphasize that high phenotypic plasticity is not per se positive for adaptation to climate change, as differences in stress responses are resulting in high phenotypic plasticity as expressed by common plasticity indices, which is likely to be related to increased mortality under stress in more plastic populations.     

How does variation in the environment and individual cognition explain the existence of consistent behavioral differences?

According to recent studies on animal personalities, the level of behavioral plasticity, which can be viewed as the slope of the behavioral reaction norm, varies among individuals, populations, and species. Still, it is conceptually unclear how the interaction between environmental variation and variation in animal cognition affect the evolution of behavioral plasticity and expression of animal personalities. Here, we (1) use literature to review how environmental variation and individual variation in cognition explain population and individual level expression of behavioral plasticity and (2) draw together empirically yet nontested, conceptual framework to clarify how these factors affect the evolution and expression of individually consistent behavior in nature. The framework is based on simple principles: first, information acquisition requires cognition that is inherently costly to build and maintain. Second, individual differences in animal cognition affect the differences in behavioral flexibility, i.e. the variance around the mean of the behavioral reaction norm, which defines plasticity. Third, along the lines of the evolution of cognition, we predict that environments with moderate variation favor behavioral flexibility. This occurs since in those environments costs of cognition are covered by being able to recognize and use information effectively. Similarly, nonflexible, stereotypic behaviors may be favored in environments that are either invariable or highly variable, since in those environments cognition does not give any benefits to cover the costs or cognition is not able to keep up with environmental change, respectively. If behavioral plasticity develops in response to increasing environmental variability, plasticity should dominate in environments that are moderately variable, and expression of animal personalities and behavioral syndromes may differ between environments. We give suggestions how to test our hypothesis and propose improvements to current behavioral testing protocols in the field of animal personality.     

Effects of predation environment and food availability on somatic growth in the Livebearing Fish Brachyrhaphis rhabdophora (Pisces: Poeciliidae)

Variation in somatic growth rates is of great interest to biologists because of the relationship between growth and other fitness‐determining traits, and it results from both genetic and environmentally induced variation (i.e. plasticity). Theoretical predictions suggest that mean somatic growth rates and the shape of the reaction norm for growth can be influenced by variation in predator‐induced mortality rates. Few studies have focused on variation in reaction norms for growth in response to resource availability between high‐predation and low‐predation environments. We used juvenile Brachyrhaphis rhabdophora from high‐predation and low‐predation environments to test for variation in mean growth rates and for variation in reaction norms for growth at two levels of food availability in a common‐environment experiment. To test for variation in growth rates in the field, we compared somatic growth rates in juveniles in high‐predation and low‐predation environments. In the common‐environment experiment, mean growth rates did not differ between fish from differing predation environments, but the interaction between predation environment and food level took the form of a crossing reaction norm for both growth in length and mass. Fish from low‐predation environments exhibited no significant difference in growth rate between high and low food treatments. In contrast, fish from high‐predation environments exhibited variation in growth rates between high and low food treatments, with higher food availability resulting in higher growth rates. In the field, individuals in the high‐predation environment grow at a faster rate than those in low‐predation environments at the smallest sizes (comparable to sizes in the common‐environment experiment). These data provide no evidence for evolved differences in mean growth rates between predation environments. However, fish from high‐predation environments exhibited greater plasticity in growth rates in response to resource availability suggesting that predation environments may exhibit increased variation in food availability for prey fish and consequent selection for plasticity.     

Individual variation in thermal plasticity and its impact on mass-scaling

Physiological processes vary widely across individuals and can influence how individuals respond to environmental change. Repeatability in how metabolic rate changes across temperatures (i.e. metabolic thermal plasticity) can influence mass-scaling exponents in different thermal environments. Moreover, repeatable plastic responses are necessary for reaction norms to respond to selective forces which is important for populations living in fluctuating environments. Nonetheless, only a small number of studies have explicitly quantified repeatability in metabolic plasticity, and fewer have explored how it can impact mass-scaling. We repeatedly measured standard metabolic rate of n = 42 delicate skinks Lampropholis delicata at six temperatures over the course of four months (N_{[observations]} = 4952). Using hierarchical statistical techniques, we accounted for multi-level variation and measurement error in our data in order to obtain more precise estimates of reaction norm repeatability and mass-scaling exponents at different acute temperatures. Our results show that individual differences in metabolic thermal plasticity were somewhat consistent over time (R_slope = 0.25, 95% CI = 2.48 × 10⁻⁸ – 0.67), however estimates were associated with a large degree of error. After accounting for measurement error, which decreased steadily with temperature, we show that among individual variance remained consistent across all temperatures. Congruently, temperature specific repeatability of average metabolic rate was stable across temperatures. Cross-temperature correlations were positive but were not uniform across the reaction norm. After taking into account multiple sources of variation, our estimates for mass-scaling did not change with temperature and were in line with published values for snakes and lizards. This implies that repeatable plastic responses may promote thermal stability of scaling exponents. Our work contributes to understanding how energy expenditure scales with abiotic and biotic factors and the capacity for reaction norms to respond to selection.     

Ecological genetics of sediment browsing behaviour in a planktonic crustacean

Zooplankton can display complex habitat selection behaviours that influence the way they interact with their environments. Some species, although primarily pelagic, can exploit sediment‐borne particles as a food source or use sediments as a refuge from pelagic predation. However, this strategy may increase the exposure to other risks such as benthic predation and infection from sediment‐borne parasite transmission stages. The evolution of habitat selection behaviour in these species is thus expected to be influenced by multiple and possibly contrasting selective forces. Here, we study the browsing behaviour of the water flea Daphnia magna on bottom sediments. First, we demonstrated genetic variation for sediment browsing among D. magna genotypes from natural populations sampled across a broad geographic range. Next, we used an F2 recombinant panel to perform a QTL analysis and identified three regions in the D. magna genome contributing to variation in browsing behaviour. We also analysed the correlation between our data and previously published data on the phototactic behaviour of genotypes from the same F2 panel. Clonal means of the two behavioral traits were not correlated, suggesting that they may evolve independently. Browsing behaviour is likely to be a relevant component of habitat selection in D. magna, and its study may help to incorporate the interactions with the sediment into eco‐evolutionary models of this key freshwater species.     

Maintenance of genetic variation in phenotypic plasticity: the role of environmental variation

We study genetic variation in phenotypic plasticity maintained by a balance between mutation and weak stabilizing selection. We consider linear reaction norms allowing for spatial and/or temporal variation in the environments of development and selection. We show that the overall genetic variation maintained does not depend on whether the trait is plastic or not. The genetic variances in height and slope of a linear reaction norm, and their covariance, are predicted to decrease with the variation in the environment. Non-pleiotropic loci influencing either height or slope are expected to decrease the genetic variance in slope relative to that in height. Decrease in the ratio of genetic variance in slope to genetic variance in height with increasing variation in the environment presents a test for the presence of loci that only influence the slope, and not the height. We use data on Drosophila to test the theory. In seven of eight pair-wise comparisons genetic variation in reaction norm is higher in a less variable environment than in a more variable environment, which is in accord with the model's predictions.     

Locally adapted traits maintained in the face of high gene flow

Gene flow between phenotypically divergent populations can disrupt local adaptation or, alternatively, may stimulate adaptive evolution by increasing genetic variation. We capitalised on historical Trinidadian guppy transplant experiments to test the phenotypic effects of increased gene flow caused by replicated introductions of adaptively divergent guppies, which were translocated from high‐ to low‐predation environments. We sampled two native populations prior to the onset of gene flow, six historic introduction sites, introduction sources and multiple downstream points in each basin. Extensive gene flow from introductions occurred in all streams, yet adaptive phenotypic divergence across a gradient in predation level was maintained. Descendants of guppies from a high‐predation source site showed high phenotypic similarity with native low‐predation guppies in as few as ~12 generations after gene flow, likely through a combination of adaptive evolution and phenotypic plasticity. Our results demonstrate that locally adapted phenotypes can be maintained despite extensive gene flow from divergent populations.     

Geographic variation in phenotypic plasticity in response to dissolved oxygen in an African cichlid fish

Genetic adaptation and phenotypic plasticity are two ways in which organisms can adapt to local environmental conditions. We examined genetic and plastic variation in gill and brain size among swamp (low oxygen; hypoxic) and river (normal oxygen; normoxic) populations of an African cichlid fish, Pseudocrenilabrus multicolor victoriae. Larger gills and smaller brains should be advantageous when oxygen is low, and we hypothesized that the relative contribution of local genetic adaptation vs. phenotypic plasticity should be related to potential for dispersal between environments (because of gene flow’s constraint on local genetic adaptation). We conducted a laboratory‐rearing experiment, with broods from multiple populations raised under high‐oxygen and low‐oxygen conditions. We found that most of the variation in gill size was because of plasticity. However, both plastic and genetic effects on brain mass were detected, as were genetic effects on brain mass plasticity. F₁ offspring from populations with the highest potential for dispersal between environments had characteristically smaller and more plastic brains. This phenotypic pattern might be adaptive in the face of gene flow, if smaller brains and increased plasticity confer higher average fitness across environment types.     

Intraspecific variation in thermal acclimation and tolerance between populations of the winter ant,Prenolepis imparis

Thermal phenotypic plasticity, otherwise known as acclimation, plays an essential role in how organisms respond to short‐term temperature changes. Plasticity buffers the impact of harmful temperature changes; therefore, understanding variation in plasticity in natural populations is crucial for understanding how species will respond to the changing climate. However, very few studies have examined patterns of phenotypic plasticity among populations, especially among ant populations. Considering that this intraspecies variation can provide insight into adaptive variation in populations, the goal of this study was to quantify the short‐term acclimation ability and thermal tolerance of several populations of the winter ant, Prenolepis imparis. We tested for correlations between thermal plasticity and thermal tolerance, elevation, and body size. We characterized the thermal environment both above and below ground for several populations distributed across different elevations within California, USA. In addition, we measured the short‐term acclimation ability and thermal tolerance of those populations. To measure thermal tolerance, we used chill‐coma recovery time (CCRT) and knockdown time as indicators of cold and heat tolerance, respectively. Short‐term phenotypic plasticity was assessed by calculating acclimation capacity using CCRT and knockdown time after exposure to both high and low temperatures. We found that several populations displayed different chill‐coma recovery times and a few displayed different heat knockdown times, and that the acclimation capacities of cold and heat tolerance differed among most populations. The high‐elevation populations displayed increased tolerance to the cold (faster CCRT) and greater plasticity. For high‐temperature tolerance, we found heat tolerance was not associated with altitude; instead, greater tolerance to the heat was correlated with increased plasticity at higher temperatures. These current findings provide insight into thermal adaptation and factors that contribute to phenotypic diversity by revealing physiological variance among populations.     

Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds

Successful urban colonization by formerly rural species represents an ideal situation in which to study adaptation to novel environments. We address this issue using candidate genes for behavioural traits that are expected to play a role in such colonization events. We identified and genotyped 16 polymorphisms in candidate genes for circadian rhythms, harm avoidance and migratory and exploratory behaviour in 12 paired urban and rural populations of the blackbird Turdus merula across the Western Palaearctic. An exonic microsatellite in the SERT gene, a candidate gene for harm avoidance behaviour, exhibited a highly significant association with habitat type in an analysis conducted across all populations. Genetic divergence at this locus was consistent in 10 of the 12 population pairs; this contrasts with previously reported stochastic genetic divergence between these populations at random markers. Our results indicate that behavioural traits related to harm avoidance and associated with the SERT polymorphism experience selection pressures during most blackbird urbanization events. These events thus appear to be influenced by homogeneous adaptive processes in addition to previously reported demographic founder events.     

Phylogeography and support vector machine classification of colour variation in panther chameleons

Lizards and snakes exhibit colour variation of adaptive value for thermoregulation, camouflage, predator avoidance, sexual selection and speciation. Furcifer pardalis, the panther chameleon, is one of the most spectacular reptilian endemic species in Madagascar, with pronounced sexual dimorphism and exceptionally large intraspecific variation in male coloration. We perform here an integrative analysis of molecular phylogeography and colour variation after collecting high‐resolution colour photographs and blood samples from 324 F. pardalis individuals in locations spanning the whole species distribution. First, mitochondrial and nuclear DNA sequence analyses uncover strong genetic structure among geographically restricted haplogroups, revealing limited gene flow among populations. Bayesian coalescent modelling suggests that most of the mitochondrial haplogroups could be considered as separate species. Second, using a supervised multiclass support vector machine approach on five anatomical components, we identify patterns in 3D colour space that efficiently predict assignment of male individuals to mitochondrial haplogroups. We converted the results of this analysis into a simple visual classification key that can assist trade managers to avoid local population overharvesting.     

Phenotypic variation in invasive and biocontrol populations of the harlequin ladybird, Harmonia axyridis

Despite numerous releases for biological control purposes during more than 20 years in Europe, Harmonia axyridis failed to become established until the beginning of the 21st century. Its status as invasive alien species is now widely recognised. Theory suggests that invasive populations should evolve toward greater phenotypic plasticity because they encounter differing environments during the invasion process. On the contrary, populations used for biological control have been maintained under artificial rearing conditions for many generations; they are hence expected to become specialised on a narrow range of environments and show lower phenotypic plasticity. Here we compared phenotypic traits and the extent of adaptive phenotypic plasticity in two invasive populations and two populations commercialized for biological control by (i) measuring six phenotypic traits related to fitness (eggs hatching rate, larval survival rate, development time, sex ratio, fecundity over 6 weeks and survival time of starving adults) at three temperatures (18, 24 and 30°C), (ii) recording the survival rate and quiescence aggregation behaviour when exposed to low temperatures (5, 10 and 15°C), and (iii) studying the cannibalistic behaviour of populations in the absence of food. Invasive and biocontrol populations displayed significantly different responses to temperature variation for a composite fitness index computed from the traits measured at 18, 24 and 30°C, but not for any of those traits considered independently. The plasticity measured on the same fitness index was higher in the two invasive populations, but this difference was not statistically significant. On the other hand, invasive populations displayed significantly higher survival and higher phenotypic plasticity when entering into quiescence at low temperatures. In addition, one invasive population displayed a singular cannibalistic behaviour. Our results hence only partly support the expectation of increased adaptive phenotypic plasticity of European invasive populations of H. axyridis, and stress the importance of the choice of the environmental parameters to be manipulated for assessing phenotypic plasticity variation among populations.