Plastic responses to novel environments are biased towards phenotype dimensions with high additive genetic variation.

Environmentally induced phenotypes have been proposed to initiate and bias adaptive evolutionary change toward particular directions. The potential for this to happen depends in part on how well plastic responses are aligned with the additive genetic variance and covariance in traits. Using meta-analysis, we demonstrate that plastic responses to novel environments tend to occur along phenotype dimensions that harbor substantial amounts of additive genetic variation. This suggests that selection for or against environmentally induced phenotypes typically will be effective. One interpretation of the alignment between the direction of plasticity and the main axis of additive genetic variation is that developmental systems tend to respond to environmental novelty as they do to genetic mutation. This makes it challenging to distinguish if the direction of evolution is biased by plasticity or genetic "constraint." Our results therefore highlight a need for new theoretical and empirical approaches to address the role of plasticity in evolution.

Developmental plasticity and evolutionary explanations.

Developmental plasticity looks like a promising bridge between ecological and developmental perspectives on evolution. Yet, there is no consensus on whether plasticity is part of the explanation for adaptive evolution or an optional "add-on" to genes and natural selection. Here, we suggest that these differences in opinion are caused by differences in the simplifying assumptions, and particular idealizations, that enable evolutionary explanation. We outline why idealizations designed to explain evolution through natural selection prevent an understanding of the role of development, and vice versa. We show that representing plasticity as a reaction norm conforms with the idealizations of selective explanations, which can give the false impression that plasticity has no explanatory power for adaptive evolution. Finally, we use examples to illustrate why evolutionary explanations that include developmental plasticity may in fact be more satisfactory than explanations that solely refer to genes and natural selection.

Social and spatial effects on genetic variation between foraging flocks in a wild bird population.

Social interactions are rarely random. In some instances, animals exhibit homophily or heterophily, the tendency to interact with similar or dissimilar conspecifics, respectively. Genetic homophily and heterophily influence the evolutionary dynamics of populations, because they potentially affect sexual and social selection. Here, we investigate the link between social interactions and allele frequencies in foraging flocks of great tits (Parus major) over three consecutive years. We constructed co-occurrence networks which explicitly described the splitting and merging of 85,602 flocks through time (fission-fusion dynamics), at 60 feeding sites. Of the 1,711 birds in those flocks, we genotyped 962 individuals at 4,701 autosomal single nucleotide polymorphisms (SNPs). By combining genomewide genotyping with repeated field observations of the same individuals, we were able to investigate links between social structure and allele frequencies at a much finer scale than was previously possible. We explicitly accounted for potential spatial effects underlying genetic structure at the population level. We modelled social structure and spatial configuration of great tit fission-fusion dynamics with eigenvector maps. Variance partitioning revealed that allele frequencies were strongly affected by group fidelity (explaining 27%-45% of variance) as individuals tended to maintain associations with the same conspecifics. These conspecifics were genetically more dissimilar than expected, shown by genomewide heterophily for pure social (i.e., space-independent) grouping preferences. Genomewide homophily was linked to spatial configuration, indicating spatial segregation of genotypes. We did not find evidence for homophily or heterophily for putative socially relevant candidate genes or any other SNP markers. Together, these results demonstrate the importance of distinguishing social and spatial processes in determining population structure.

Genetics and developmental biology of cooperation.

Despite essential progress towards understanding the evolution of cooperative behaviour, we still lack detailed knowledge about its underlying molecular mechanisms, genetic basis, evolutionary dynamics and ontogeny. An international workshop "Genetics and Development of Cooperation," organized by the University of Bern (Switzerland), aimed at discussing the current progress in this research field and suggesting avenues for future research. This review uses the major themes of the meeting as a springboard to synthesize the concepts of genetic and nongenetic inheritance of cooperation, and to review a quantitative genetic framework that allows for the inclusion of indirect genetic effects. Furthermore, we argue that including nongenetic inheritance, such as transgenerational epigenetic effects, parental effects, ecological and cultural inheritance, provides a more nuanced view of the evolution of cooperation. We summarize those genes and molecular pathways in a range of species that seem promising candidates for mechanisms underlying cooperative behaviours. Concerning the neurobiological substrate of cooperation, we suggest three cognitive skills necessary for the ability to cooperate: (i) event memory, (ii) synchrony with others and (iii) responsiveness to others. Taking a closer look at the developmental trajectories that lead to the expression of cooperative behaviours, we discuss the dichotomy between early morphological specialization in social insects and more flexible behavioural specialization in cooperatively breeding vertebrates. Finally, we provide recommendations for which biological systems and species may be particularly suitable, which specific traits and parameters should be measured, what type of approaches should be followed, and which methods should be employed in studies of cooperation to better understand how cooperation evolves and manifests in nature.

To graze or gorge: consistency and flexibility of individual foraging tactics in tits.

An individual's foraging behaviour and time allocated to feeding have direct consequences for its fitness. Despite much research on population-level foraging decisions, few studies have investigated individual differences in fine-scale daily foraging patterns among wild animals. Here, we explore the consistency and plasticity of feeding tactics of individual great tits (Parus major) and blue tits (Cyanistes caeruleus), using a grid of 65 automated feeding stations in a 385-ha woodland, during three winters. We use a principal component analysis to describe individual variation in six feeding parameters and examine how these differences covary with dominance-linked attributes (species, age and sex), the personality trait 'exploration behaviour', distance to territory and local competition intensity. Analysis of 933 086 feeder visits by 3134 individuals revealed that the majority of variation in the timing of feeding was explained by two principal components. PC1 ('binge-eating'), accounting for 38% of variation, captured temporal clustering of feeding, with high repeatability both within and between years (r range: 0·42-0·55). PC2 ('transience'), accounting for 27% of variance, described how much individuals used feeders and was also repeatable (r: 0·34-0·62). While exhibiting consistent individual differences, birds also showed flexibility in foraging patterns, binge-eating less and using feeders more when they experienced greater local competition. Individuals in behaviourally dominant states (great tits, males and adults) binged more than subordinate birds (blue tits, females and juveniles) when their territories were distant from feeding stations. Moreover, great tits and males used feeders more than blue tits and females respectively, while birds feeding further from their territory used feeders less than those feeding closer. 'Exploration behaviour' was unrelated to both measures of daily foraging behaviour. This study presents some of the first evidence that birds use consistent alternative foraging tactics at a fine temporal scale. Individuals are consistent in their tactics, and also adjust their foraging behaviour with changes in local competition. Hence, studies of foraging behaviour should consider the extent to which such individual-level variability in foraging behaviour is under selection.

Environmentally induced DNA methylation is inherited across generations in an aquatic keystone species.

Transgenerational inheritance of environmentally induced epigenetic marks can have significant impacts on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. We used whole-genome bisulfite sequencing of individual water fleas (Daphnia magna) to assess whether environmentally induced DNA methylation is transgenerationally inherited. Genetically identical females were exposed to one of three natural stressors, or a de-methylating drug, and their offspring were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) in F1 individuals whose mothers were exposed to a natural stressor. Roughly half of these environmentally induced DMPs persisted until generation F4. In contrast, treatment with the drug demonstrated that pervasive hypomethylation upon exposure is reset almost completely after one generation. These results suggest that environmentally induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of freshwater communities.

Plasticity leaves a phenotypic signature during local adaptation.

Phenotypic responses to a novel or extreme environment are initially plastic, only later to be followed by genetic change. Whether or not environmentally induced phenotypes are sufficiently recurrent and fit to leave a signature in adaptive evolution is debated. Here, we analyze multivariate data from 34 plant reciprocal transplant studies to test: (1) if plasticity is an adaptive source of developmental bias that makes locally adapted populations resemble the environmentally induced phenotypes of ancestors; and (2) if plasticity, standing phenotypic variation and genetic divergence align during local adaptation. Phenotypic variation increased marginally in foreign environments but, as predicted, the direction of ancestral plasticity was generally well aligned with the phenotypic difference between locally adapted populations, making plasticity appear to "take the lead" in adaptive evolution. Plastic responses were sometimes more extreme than the phenotypes of locally adapted plants, which can give the impression that plasticity and evolutionary adaptation oppose each other; however, environmentally induced and locally adapted phenotypes were rarely misaligned. Adaptive fine-tuning of phenotypes-genetic accommodation-did not fall along the main axis of standing phenotypic variation or the direction of plasticity, and local adaptation did not consistently modify the direction or magnitude of plasticity. These results suggest that plasticity is a persistent source of developmental bias that shapes how plant populations adapt to environmental change, even when plasticity does not constrain how populations respond to selection.

Plasticity and evolutionary convergence in the locomotor skeleton of Greater Antillean Anolis lizards.

Plasticity can put evolution on repeat if development causes species to generate similar morphologies in similar environments. Anolis lizards offer the opportunity to put this role of developmental plasticity to the test. Following colonization of the four Greater Antillean islands, Anolis lizards independently and repeatedly evolved six ecomorphs adapted to manoeuvring different microhabitats. By quantifying the morphology of the locomotor skeleton of 95 species, we demonstrate that ecomorphs on different islands have diverged along similar trajectories. However, microhabitat-induced morphological plasticity differed between species and did not consistently improve individual locomotor performance. Consistent with this decoupling between morphological plasticity and locomotor performance, highly plastic features did not show greater evolvability, and plastic responses to microhabitat were poorly aligned with evolutionary divergence between ecomorphs. The locomotor skeleton of Anolis may have evolved within a subset of possible morphologies that are highly accessible through genetic change, enabling adaptive convergence independently of plasticity.

Timing of maternal exposure to toxic cyanobacteria and offspring fitness in Daphnia magna: Implications for the evolution of anticipatory maternal effects.

Organisms that regularly encounter stressful environments are expected to use cues to develop an appropriate phenotype. Water fleas (Daphnia spp.) are exposed to toxic cyanobacteria during seasonal algal blooms, which reduce growth and reproductive investment. Because generation time is typically shorter than the exposure to cyanobacteria, maternal effects provide information about the local conditions subsequent generations will experience. Here, we evaluate if maternal effects in response to microcystin, a toxin produced by cyanobacteria, represent an inheritance system evolved to transmit information in Daphnia magna. We exposed mothers as juveniles and/or as adults, and tested the offspring's fitness in toxic and non-toxic environments. Maternal exposure until reproduction reduced offspring fitness, both in the presence and in the absence of toxic cyanobacteria. However, this effect was accompanied by a small positive fitness effect, relative to offspring from unexposed mothers, in the presence of toxic cyanobacteria. This effect was mainly elicited in response to maternal exposure to toxic cyanobacteria early in life and less so during reproduction. None of these effects were explained by changes in egg size. A meta-analysis using our and others' experiments suggests that the adaptive value of maternal effects to cyanobacteria exposure is weak at best. We suggest that the beneficial maternal effect in our study is an example of phenotypic accommodation spanning generations, rather than a mechanism evolved to transmit information about cyanobacteria presence between generations.

Low Incubation Temperature Induces DNA Hypomethylation in Lizard Brains.

Developmental stress can have organizational effects on suites of physiological, morphological, and behavioral characteristics. In lizards, incubation temperature is perhaps the most significant environmental variable affecting embryonic development. Wall lizards (Podarcis muralis) recently introduced by humans from Italy to England experience stressfully cool incubation conditions, which we here show reduce growth and increase the incidence of scale malformations. Using a methylation-sensitive AFLP protocol optimized for vertebrates, we demonstrate that this low incubation temperature also causes hypomethylation of DNA in brain tissue. A consistent pattern across methylation-susceptible AFLP loci suggests that hypomethylation is a general response and not limited to certain CpG sites. The functional consequences of hypomethylation are unknown, but it could contribute to genome stability and regulation of gene expression. Further studies of the effects of incubation temperature on DNA methylation in ectotherm vertebrates may reveal mechanisms that explain why the embryonic thermal environment often has physiological and behavioral consequences for offspring.