Plasticity and evolution in correlated suites of traits

When organisms are faced with new or changing environments, a central challenge is the coordination of adaptive shifts in many different phenotypic traits. Relationships among traits may facilitate or constrain evolutionary responses to selection, depending on whether the direction of selection is aligned or opposed to the pattern of trait correlations. Attempts to predict evolutionary potential in correlated traits generally assume that correlations are stable across time and space; however, increasing evidence suggests that this may not be the case, and flexibility in trait correlations could bias evolutionary trajectories. We examined genetic and environmental influences on variation and covariation in a suite of behavioural traits to understand if and how flexibility in trait correlations influences adaptation to novel environments. We tested the role of genetic and environmental influences on behavioural trait correlations by comparing Trinidadian guppies (Poecilia reticulata) historically adapted to high‐ and low‐predation environments that were reared under native and non‐native environmental conditions. Both high‐ and low‐predation fish exhibited increased behavioural variance when reared under non‐native vs. native environmental conditions, and rearing in the non‐native environment shifted the major axis of variation among behaviours. Our findings emphasize that trait correlations observed in one population or environment may not predict correlations in another and that environmentally induced plasticity in correlations may bias evolutionary divergence in novel environments.     

Predation mediated population divergence in complex behaviour of nine‐spined stickleback (Pungitius pungitius)

The proximate and ultimate explanations for behavioural syndromes (correlated behaviours – a population trait) are poorly understood, and the evolution of behavioural types (configuration of behaviours – an individual trait) has been rarely studied. We investigated population divergence in behavioural syndromes and types using individually reared, completely predator‐ or conspecific‐naïve adult nine‐spined sticklebacks (Pungitius pungitius) from two marine and two predatory fish free, isolated pond populations. We found little evidence for the existence of behavioural syndromes, but population divergence in behavioural types was profound: individuals from ponds were quicker in feeding, bolder and more aggressive than individuals from marine environments. Our data reject the hypothesis that behavioural syndromes exist as a result of genetic correlations between behavioural traits, and support the contention that different behavioural types can be predominant in populations differing in predation pressure, most probably as a result of repeated independent evolution of separate behavioural traits.     

Heritability and genetic correlations of personality traits in a wild population of yellow‐bellied marmots (Marmota flaviventris)

Describing and quantifying animal personality is now an integral part of behavioural studies because individually distinctive behaviours have ecological and evolutionary consequences. Yet, to fully understand how personality traits may respond to selection, one must understand the underlying heritability and genetic correlations between traits. Previous studies have reported a moderate degree of heritability of personality traits, but few of these studies have either been conducted in the wild or estimated the genetic correlations between personality traits. Estimating the additive genetic variance and covariance in the wild is crucial to understand the evolutionary potential of behavioural traits. Enhanced environmental variation could reduce heritability and genetic correlations, thus leading to different evolutionary predictions. We estimated the additive genetic variance and covariance of docility in the trap, sociability (mirror image stimulation), and exploration and activity in two different contexts (open‐field and mirror image simulation experiments) in a wild population of yellow‐bellied marmots (Marmota flaviventris). We estimated both heritability of behaviours and of personality traits and found nonzero additive genetic variance in these traits. We also found nonzero maternal, permanent environment and year effects. Finally, we found four phenotypic correlations between traits, and one positive genetic correlation between activity in the open‐field test and sociability. We also found permanent environment correlations between activity in both tests and docility and exploration in the MIS test. This is one of a handful of studies to adopt a quantitative genetic approach to explain variation in personality traits in the wild and, thus, provides important insights into the potential variance available for selection.     

Changes in behavioural trait integration following rapid ecotype divergence in an aquatic isopod

Colonization of new habitats can relax selection pressures, and traits or trait combinations no longer selected for might become reduced or lost. We investigated behavioural differentiation and behavioural trait integration in the freshwater isopod Asellus aquaticus. This isopod has recently colonized a novel habitat and diverged into two ecotypes which encounter different predator faunas. We investigated sex-specific behavioural differences and phenotypic integration in three behavioural assays: (i) time to emerge (TE) from a shelter, (ii) activity and (iii) escape behaviour. General activity and escape behaviour differed between ecotypes. Furthermore, general activity and TE differed between sexes. Behavioural traits were more frequently correlated in the ancestral habitat, and phenotypic integration tended to be higher in this habitat as well. Our study suggests that different predator types, but also other ecological factors such as habitat matrices and population densities, might explain the differences in behavioural integration in these ecotypes.     

A strong genetic correlation underlying a behavioural syndrome disappears during development because of genotype–age interactions

In animal populations, as in humans, behavioural differences between individuals that are consistent over time and across contexts are considered to reflect personality, and suites of correlated behaviours expressed by individuals are known as behavioural syndromes. Lifelong stability of behavioural syndromes is often assumed, either implicitly or explicitly. Here, we use a quantitative genetic approach to study the developmental stability of a behavioural syndrome in a wild population of blue tits. We find that a behavioural syndrome formed by a strong genetic correlation of two personality traits in nestlings disappears in adults, and we demonstrate that genotype–age interaction is the likely mechanism underlying this change during development. A behavioural syndrome may hence change during organismal development, even when personality traits seem to be strongly physiologically or functionally linked in one age group. We outline how such developmental plasticity has important ramifications for understanding the mechanistic basis as well as the evolutionary consequences of behavioural syndromes.     

Natural selection,plasticity and the emergence of a behavioural syndrome in the wild

Individuals often show consistent behavioural differences where behaviours can form integrated units across functionally different contexts. However, the factors causing and maintaining behavioural syndromes in natural populations remain poorly understood. In this study, we provide evidence for the emergence of a behavioural syndrome during the first months of life in wild brown trout (Salmo trutta). Behavioural traits of trout were scored before and after a 2‐month interval covering a major survival bottleneck, whereupon the consistency and covariance of behaviours were analysed. We found that selection favoured individuals with high activity levels in an open‐field context, a personality trait consistent throughout the duration of the experiment. In addition, a behavioural syndrome emerged over the 2 months in the wild, linking activity to aggressiveness and exploration tendency. These novel results suggest that behavioural syndromes can emerge rapidly in nature from interaction between natural selection and behavioural plasticity affecting single behaviours.     

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.     

Population differences in behaviour are explained by shared within‐population trait correlations

Correlations in behavioural traits across time, situation and ecological context (i.e. ‘behavioural syndromes’ or ‘personality’) have been documented for a variety of behaviours, and in diverse taxa. Perhaps the most controversial inference from the behavioural syndromes literature is that correlated behaviour may act as an evolutionary constraint and evolutionary change in one’s behaviour may necessarily involve shifts in others. We test the two predictions of this hypothesis using comparative data from eighteen populations of the socially polymorphic spider, Anelosimus studiosus (Araneae, Theriidae). First, we ask whether geographically distant populations share a common syndrome. Second, we test whether population differences in behaviour are correlated similarly to within‐population trait correlations. Our results reveal that populations separated by as much as 36° latitude shared similar syndromes. Furthermore, population differences in behaviour were correlated in the same manner as within‐population trait correlations. That is, population divergence tended to be along the same axes as within‐population covariance. Together, these results suggest a lack of evolutionary independence in the syndrome’s constituent traits.     

Rapid divergence of animal personality and syndrome structure across an arid-aquatic habitat matrix

Intraspecific trait variation, including animal personalities and behavioural syndromes, affects how individual animals and populations interact with their environment. Within-species behavioural variation is widespread across animal taxa, which has substantial and unexplored implications for the ecological and evolutionary processes of animals. Accordingly, we sought to investigate individual behavioural characteristics in several populations of a desert-dwelling fish, the Australian desert goby (Chlamydogobius eremius). We reared first generation offspring in a common garden to compare non-ontogenic divergence in behavioural phenotypes between genetically interconnected populations from contrasting habitats (isolated groundwater springs versus hydrologically variable river waterholes). Despite the genetic connectedness of populations, fish had divergent bold-exploratory traits associated with their source habitat. This demonstrates divergence in risk-taking traits as a rapid phenotypic response to ecological pressures in arid aquatic habitats: neophilia may be suppressed by increased predation pressure and elevated by high intraspecific competition. Correlations between personality traits also differed between spring and river fish. River populations showed correlations between dispersal and novel environment behaviours, revealing an adaptive behavioural syndrome (related to dispersal and exploration) that was not found in spring populations. This illustrates the adaptive significance of heritable behavioural variation within and between populations, and their importance to animals persisting across contrasting habitats.     

Contemporary Parallel Diversification,Antipredator Adaptations and Phenotypic Integration in an Aquatic Isopod

It is increasingly being recognized that predation can be a strong diversifying agent promoting ecological divergence. Adaptations against different predatory regimes can emerge over short periods of time and include many different traits. We studied antipredator adaptations in two ecotypes of an isopod (Asellus aquaticus) that have, diverged in parallel in two Swedish lakes over the last two decades. We quantified differences in escape speed, morphology and behavior for isopods from different ecotypes present in these lakes. Isopods from the source habitat (reed) coexist with mainly invertebrate predators. They are more stream-profiled and have higher escape speeds than isopods in the newly colonized stonewort habitat, which has higher density of fish predators. Stonewort isopods also show more cautious behaviors and had higher levels of phenotypic integration between coloration and morphological traits than the reed isopods. Colonization of a novel habitat with a different predation regime has thus strengthened the correlations between pigmentation and morphology and weakened escape performance. The strong signature of parallelism for these phenotypic traits indicates that divergence is likely to be adaptive and is likely to have been driven by differences in predatory regimes. Furthermore, our results indicate that physical performance, behavior and morphology can change rapidly and in concert as new habitats are colonized.     

MULTIVARIATE ANALYSIS OF SELECTION IN EXPERIMENTAL POPULATIONS DERIVED FROM HYBRIDIZATION OF TWO ECOTYPES OF THE ANNUAL PLANT DIODIA TERES W. (RUBIACEAE)

Morphologically variable F₂ genotypes derived from hybridization of coastal and inland ecotypes of the annual plant Diodia teres were used to identify selection on morphological traits in the natural habitat of each ecotype. These ecotypes occur in very different habitats, and have evolved pronounced morphological differentiation. Selection analysis can suggest whether present patterns of selection can explain morphological differences between ecotypes. F₂ genotypes were characterized morphologically, clonally replicated, and transplanted into the habitat of each ecotype. Selection was measured on six morphological traits. Directional and stabilizing selection occurred on many traits; direction and strength of selection varied sharply at different stages of growth, as revealed by a path-analysis approach that divided selection into a set of independent components. Directional selection favored traits of the native population at the coastal habitat, but less so at the inland habitat. Selection was of sufficient strength to create the observed morphological differences between ecotypes in 25–100 generations, given constant selection and sufficient genetic variation. In effects on fitness, most traits were neither independent nor consistently interactive with other traits. Rather, many traits entered into strong but evanescent interactions affecting particular components of fitness. Observed interactions did not support the hypothesis that the morphology of each ecotype was functionally integrated to a high degree.     

Correlational selection does not explain the evolution of a behavioural syndrome

Correlated suites of behaviours, or behavioural syndromes, appear to be widespread, and yet few studies have explored how they arise and are maintained. One possibility holds that correlational selection can generate and maintain behavioural syndrome if certain behavioural combinations enjoy greater fitness than other combinations. Here we test this correlational selection hypothesis by comparing behavioural syndrome structure with a multivariate fitness surface based on reproductive success of male water striders. We measured the structure of a behavioural syndrome including dispersal ability, exploration behaviour, latency to remount and sex recognition sensitivity in males. We then measured the relationship between these behaviours and mating success in a range of sex ratio environments. Despite the presence of some significant correlational selection, behavioural syndrome structure was not associated with correlational selection on behaviours. Although we cannot conclusively reject the correlational selection hypothesis, our evidence suggests that correlational selection and resulting linkage disequilibrium might not be responsible for maintaining the strong correlations between behaviours. Instead, we suggest alternative ways in which this behavioural syndrome may have arisen and outline the need for physiological and quantitative genetic tests of these suggestions.     

Bud phenology and growth are subject to divergent selection across a latitudinal gradient in Populus angustifolia and impact adaptation across the distributional range and associated arthropods

Temperate forest tree species that span large geographical areas and climatic gradients often have high levels of genetic variation. Such species are ideal for testing how neutral demographic factors and climate‐driven selection structure genetic variation within species, and how this genetic variation can affect ecological communities. Here, we quantified genetic variation in vegetative phenology and growth traits in narrowleaf cottonwood, Populus angustifolia, using three common gardens planted with genotypes originating from source populations spanning the species' range along the Rocky Mountains of North America (ca. 1700 km). We present three main findings. First, we found strong evidence of divergent selection (Q_ST > F_ST) on fall phenology (bud set) with adaptive consequences for frost avoidance. We also found evidence for selection on bud flush duration, tree height, and basal diameter, resulting in population differentiation. Second, we found strong associations with climate variables that were strongly correlated with latitude of origin. More strongly differentiated traits also showed stronger climate correlations, which emphasizes the role that climate has played in divergent selection throughout the range. We found population × garden interaction effects; for some traits, this accounted for more of the variance than either factor alone. Tree height was influenced by the difference in climate of the source and garden locations and declined with increasing transfer distance. Third, growth traits were correlated with dependent arthropod community diversity metrics. Synthesis. Overall, we conclude that climate has influenced genetic variation and structure in phenology and growth traits and leads to local adaptation in P. angustifolia, which can then impact dependent arthropod species. Importantly, relocation of genotypes far northward or southward often resulted in poor growth, likely due to a phenological mismatch with photoperiod, the proximate cue for fall growth cessation. Genotypes moved too far southward suffer from early growth cessation, whereas those moved too far northward are prone to fall frost and winter dieback. In the face of current and forecasted climate change, habitat restoration, forestry, and tree breeding efforts should utilize these findings to better match latitudinal and climatic source environments with management locations for optimal future outcomes.     

Adaptive differentiation in floral traits in the presence of high gene flow in scarlet gilia (Ipomopsis aggregata)

Plant–pollinator interactions are thought to be major drivers of floral trait diversity. However, the relative importance of divergent pollinator‐mediated selection vs. neutral processes in floral character evolution has rarely been explored. We tested for adaptive floral trait evolution by comparing differentiation at neutral genetic loci to differentiation at quantitative floral traits in a putative Ipomopsis aggregata hybrid zone. Typical I. aggregata subsp. candida displays slender white tubular flowers that are typical of flowers pollinated by hawkmoths, and subsp. collina displays robust red tubular flowers typical of flowers pollinated by hummingbirds; yet, hybrid flower morphs are abundant across the East Slope of the Colorado Rockies. We estimated genetic differentiation (F_ST) for nuclear and chloroplast microsatellite loci and used a half‐sib design to calculate quantitative trait divergence (Q_ST) from collection sites across the morphological hybrid zone. We found little evidence for population structure and estimated mean F_ST to be 0.032. Q_ST values for several floral traits including corolla tube length and width, colour, and nectar volume were large and significantly greater than mean F_ST. We performed multivariate comparisons of neutral loci to genetic correlations within and between populations and found a strong signal for divergent selection, suggesting that specific combinations of floral display and reward traits may be the targets of selection. Our results show little support for historical subspecies categories, yet floral traits are more diverged than expected due to drift alone. Non‐neutral divergence for multivariate quantitative traits suggests that selection by pollinators is maintaining a correlation between display and reward traits.     

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.     

Diversifying selection drives parallel evolution of gill raker number and body size along the speciation continuum of European whitefish

Adaptive radiation is the evolution of ecological and phenotypical diversity. It arises via ecological opportunity that promotes the exploration of underutilized or novel niches mediating specialization and reproductive isolation. The assumed precondition for rapid local adaptation is diversifying natural selection, but random genetic drift could also be a major driver of this process. We used 27 populations of European whitefish (Coregonus lavaretus) from nine lakes distributed in three neighboring subarctic watercourses in northern Fennoscandia as a model to test the importance of random drift versus diversifying natural selection for parallel evolution of adaptive phenotypic traits. We contrasted variation for two key adaptive phenotypic traits correlated with resource utilization of polymorphic fish; the number of gill rakers and the total length of fish, with the posterior distribution of neutral genetic differentiation from 13 microsatellite loci, to test whether the observed phenotypic divergence could be achieved by random genetic drift alone. Our results show that both traits have been under diversifying selection and that the evolution of these morphs has been driven by isolation through habitat adaptations. We conclude that diversifying selection acting on gill raker number and body size has played a significant role in the ongoing adaptive radiation of European whitefish morphs in this region.     

Rapid adaptive divergence between ecotypes of an aquatic isopod inferred from FST–QST analysis

Divergent natural selection is often thought to be the principal factor driving phenotypic differentiation between populations. We studied two ecotypes of the aquatic isopod Asellus aquaticus which have diverged in parallel in several Swedish lakes. In these lakes, isopods from reed belts along the shores colonized new stonewort stands in the centre of the lakes and rapid phenotypic changes in size and pigmentation followed after colonization. We investigated if selection was likely to be responsible for these observed phenotypic changes using indirect inferences of selection (F_ST–Q_ST analysis). Average Q_ST for seven quantitative traits were higher than the average F_ST between ecotypes for putatively neutral markers (AFLPs). This suggests that divergent natural selection has played an important role during this rapid diversification. In contrast, the average Q_ST between the different reed ecotype populations was not significantly different from the mean F_ST. Genetic drift could therefore not be excluded as an explanation for the minor differences between allopatric populations inhabiting the same source habitat. We complemented this traditional F_ST–Q_ST approach by comparing the F_ST distributions across all loci (n = 67–71) with the Q_ST for each of the seven traits. This analysis revealed that pigmentation traits had diverged to a greater extent and at higher evolutionary rates than size‐related morphological traits. In conclusion, this extended and detailed type of F_ST–Q_ST analysis provides a powerful method to infer adaptive phenotypic divergence between populations. However, indirect inferences about the operation of divergent selection should be analyzed on a per‐trait basis and complemented with detailed ecological information.     

Genetic trade-off between abilities to avoid attack and to mate: a cost of tonic immobility

Consistent individual differences in correlated behaviours across contexts or situations, that is, behavioural syndromes, have recently been identified as an important factor shaping the evolution of behavioural traits, because of their potential for explaining trade-offs in behavioural responses. We examined a genetic link between abilities to mate and to avoid predation from the viewpoint of two genetically correlated behavioural traits; tonic immobility (TI), which is considered to be an antipredator behaviour, and activity levels in the red flour beetle, Tribolium castaneum. Males derived from two strains artificially selected for divergent durations of TI were used in the present study: the L strain (with longer duration and higher frequency of TI) and the S strain (shorter duration and lower frequency of TI). We found that males of the L strain had higher survival rates in predatory environments than those of the S strain, and lower mating success even in predator-free environments. To our knowledge, this is the first empirical study showing a genetic trade-off between abilities to mate and to avoid predation in relation to behavioural syndromes, using individuals exhibiting different behavioural strategies.     

Reaction norms of Arabidopsis. V. Flowering time controls phenotypic architecture in response to nutrient stress

The evolutionary and environmental stability of character correlations has increasingly been the focus of ecological and quantitative genetic studies. Although the genetic stability of character correlations is a central assumption of quantitative genetic models of phenotypic evolution, theoretical considerations suggest that both the genetic and the phenotypic architecture should change in response to selection and to environmental heterogeneity. We investigate genetic (population) differences and plasticity to nutrient availability of the phenotypic architecture describing the whole-plant phenotype of Arabidopsis thaliana (Brassicaceae). We found significant genetic differences among early and late flowering ecotypes in the relationships between several traits, when a path-analytical model was used to estimate character correlations. Furthermore, we found significant plasticity of several path coefficients when nutrient levels were altered. A whole-plant analysis considering all paths in the model simultaneously confirmed that populations of A. thaliana are characterized by distinct phenotypic architectures, and that these are altered in different ways by environmental changes. We discuss the implications of these findings for our understanding of selective pressure on and response by multivariate phenotypes.     

Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping

To identify the ecological and genetic mechanisms of local adaptation requires estimating selection on traits, identifying their genetic basis, and evaluating whether divergence in adaptive traits is due to conditional neutrality or genetic trade‐offs. To this end, we conducted field experiments for three years using recombinant inbred lines (RILs) derived from two ecotypes of Arabidopsis thaliana (Italy, Sweden), and at each parental site examined selection on flowering time and mapped quantitative trait loci (QTL). There was strong selection for early flowering in Italy, but weak selection in Sweden. Eleven distinct flowering time QTL were detected, and for each the Italian genotype caused earlier flowering. Twenty‐seven candidate genes were identified, two of which (FLC and VIN3) appear under major flowering time QTL in Italy. Seven of eight QTL in Italy with narrow credible intervals colocalized with previously reported fitness QTL, in comparison to three of four in Sweden. The results demonstrate that the magnitude of selection on flowering time differs strikingly between our study populations, that the genetic basis of flowering time variation is multigenic with some QTL of large effect, and suggest that divergence in flowering time between ecotypes is due mainly to conditional neutrality.