DENSITY DEPENDENCE AND UNPREDICTABLE SELECTION IN A HETEROGENEOUS ENVIRONMENT: COMPROMISE AND POLYMORPHISM IN THE ESS REACTION NORM

In quantitative genetic models of the evolution of reaction norms, an individual is selected in the habitat in which it develops; as a consequence, selection leads to the optimum phenotype in each habitat. Here, individuals are assumed to experience unpredictable habitat change between development and selection, so that the environment in which an individual is selected may differ from the environment in which it developed. The model reveals that unpredictability of the selection an individual actually faces leads to the evolutionarily stable bet-hedging reaction norm constituting a compromise between the phenotypic optima in the different patches. We also examine the effect of local density regulation before selection, in the patches in which the individuals develop, and after selection, in the patches in which they are selected. Density regulation before selection has a much lower influence on the evolution of the reaction norm than density regulation after selection. The source-sink structure of the environment caused by differential productivity of patches strongly affects how the compromise bet-hedging strategy weighs the different phenotypic optima and might compromise the local evolutionary stability of the evolved reaction norm. If the strength and variability among patches of density regulation after selection is sufficiently large, no single reaction norm is evolutionary stable: Polymorphic reaction norms constitute the evolutionarily stable population. We also show that a polymorphic reaction norm is more likely to be observed in a less productive habitat. The relations between the present model and the Dempster and the Levene models are discussed.     

Unpredictable selection in a structured population leads to local genetic differentiation in evolved reaction norms

Unpredictability during development of the optimum phenotype under future selection leads to a compromise reaction norm with a slope that is shallower than the slope of the optimum reaction norm. Unpredictability of selection can lead to an evolved curved reaction norm when genetic variation for curvature is available even if the optimum reaction norm is linear. This requires asymmetry in the frequency distribution of the habitats of selection; at small population size, stochasticity in the number of individuals per selection habitat is sufficient to generate such asymmetry. Unpredictability of selection in structured populations leads to local genetic differentiation of reaction norms. The mean habitat of a subpopulation is defined as the subpopulation's focal habitat. The evolved mean reaction norm of each subpopulation is anchored at the optimum genotypic value in its focal habitat. Linear reaction norms are parallel if the conditional distribution of adults around the focal habitats is the same for each subpopulation. Adult migration and absence of zygote dispersal represents the ultimate structured population, each habitat playing the role of focal habitat. Absence of zygote dispersal requires that the flow of individuals through the habitats is used instead of the habitats’ frequencies in the prediction of the evolved reaction norm. Adult migration in absence of zygote dispersal leads to an evolved pattern of locally differentiated reaction norms with optimum genotypic value anchored in the focal habitat and, for linear reaction norms, parallel slopes.     

The evolution of environmental and genetic sex determination in fluctuating environments

Twenty years ago, Bulmer and Bull suggested that disruptive selection, produced by environmental fluctuations, can result in an evolutionary transition from environmental sex determination (ESD) to genetic sex determination (GSD). We investigated the feasibility of such a process, using mutation-limited adaptive dynamics and individual-based computer simulations. Our model describes the evolution of a reaction norm for sex determination in a metapopulation setting with partial migration and variation in an environmental variable both within and between local patches. The reaction norm represents the probability of becoming a female as a function of environmental state and was modeled as a sigmoid function with two parameters, one giving the location (i.e., the value of the environmental variable for which an individual has equal chance of becoming either sex) and the other giving the slope of the reaction norm for that environment. The slope can be interpreted as being set by the level of developmental noise in morph determination, with less noise giving a steeper slope and a more switchlike reaction norm. We found convergence stable reaction norms with intermediate to large amounts of developmental noise for conditions characterized by low migration rates, small differential competitive advantages between the sexes over environments, and little variation between individual environments within patches compared to variation between patches. We also considered reaction norms with the slope parameter constrained to a high value, corresponding to little developmental noise. For these we found evolutionary branching in the location parameter and a transition from ESD toward GSD, analogous to the original analysis by Bulmer and Bull. Further evolutionary change, including dominance evolution, produced a polymorphism acting as a GSD system with heterogamety. Our results point to the role of developmental noise in the evolution of sex determination.     

Neuroendocrine control of life histories: what do we need to know to understand the evolution of phenotypic plasticity?

Almost all life histories are phenotypically plastic: that is, life-history traits such as timing of breeding, family size or the investment in individual offspring vary with some aspect of the environment, such as temperature or food availability. One approach to understanding this phenotypic plasticity from an evolutionary point of view is to extend the optimality approach to the range of environments experienced by the organism. This approach attempts to understand the value of particular traits in terms of the selection pressures that act on them either directly or owing to trade-offs due to resource allocation and other factors such as predation risk. Because these selection pressures will between environments, the predicted optimal phenotype will too. The relationship expressing the optimal phenotype for different environments is the optimal reaction norm and describes the optimal phenotypic plasticity. However, this view of phenotypic plasticity ignores the fact that the reaction norm must be underlain by some sort of control system: cues about the environment must be collected by sense organs, integrated into a decision about the appropriate life history, and a message sent to the relevant organs to implement that decision. In multicellular animals, this control mechanism is the neuroendocrine system. The central question that this paper addresses is whether the control system affects the reaction norm that evolves. This might happen in two different ways: first, the control system will create constraints on the evolution of reaction norms if it cannot be configured to produce the optimal reaction norm and second, the control system will create additional selection pressures on reaction norms if the neuroendocrine system is costly. If either of these happens, a full understanding of the way in which selection shapes reaction norms must include details of the neuroendocrine control system. This paper presents the conceptual framework needed to explain what is meant by a constraint or cost being created by the neuroendocrine system and discusses the extent to which this occurs and some possible examples. The purpose of doing this is to encourage endocrinologists to take a fresh look at neuroendocrine mechanisms and help identify the properties of the system and situations in which these generate constraints and costs that impinge on the evolution of phenotypic plasticity.     

Adaptation and constraint in the evolution of environmental sex determination

When environments differentially influence male and female performance, environmental sex determination (ESD) might evolve. The conclusion from several previous theoretical models was that reaction norms for sex determination should have a single, sharp threshold, with only females being produced in some environments and only males in others. These reaction norms can be disadvantageous in fluctuating environments, however, because they lead to sex-ratio fluctuations. We analysed the evolution of ESD, looking for equilibrium strategies in unconstrained as well as constrained strategy spaces. We identified situations where a single-threshold reaction norm is not evolutionarily stable. In these cases, we found stable strategies in the form of complex reaction norms, showing an oscillatory pattern of sex determination with respect to variation in an environmental variable. Considering that constraints could prevent such phenotypes from being realized, we found that certain randomized reaction norms, with probabilistic sex determination for a range of environments, would achieve nearly the same fitness. We also investigated reaction norms constrained to have a single threshold and found that genetic polymorphism in the environmental threshold value could evolve, producing a similar effect as a randomized reaction norm. We argue that the appearance of genetic variation can be regarded as an alternative outcome when constraints prevent the evolution of a more complex or a randomized strategy.     

Thermal plasticity of growth and development varies adaptively among alternative developmental pathways

Polyphenism, the expression of discrete alternative phenotypes, is often a consequence of a developmental switch. Physiological changes induced by a developmental switch potentially affect reaction norms, but the evolution and existence of alternative reaction norms remains poorly understood. Here, we demonstrate that, in the butterfly Pieris napi (Lepidoptera: Pieridae), thermal reaction norms of several life history traits vary adaptively among switch‐induced alternative developmental pathways of diapause and direct development. The switch was affected both by photoperiod and temperature, ambient temperature during late development having the potential to override earlier photoperiodic cues. Directly developing larvae had higher development and growth rates than diapausing ones across the studied thermal gradient. Reaction norm shapes also differed between the alternative developmental pathways, indicating pathway‐specific selection on thermal sensitivity. Relative mass increments decreased linearly with increasing temperature and were higher under direct development than diapause. Contrary to predictions, population phenology did not explain trait variation or thermal sensitivity, but our experimental design probably lacks power for finding subtle phenology effects. We demonstrate adaptive differentiation in thermal reaction norms among alternative phenotypes, and suggest that the consequences of an environmentally dependent developmental switch primarily drive the evolution of alternative thermal reaction norms in P. napi.     

Evolution of environmental cues for phenotypic plasticity

Phenotypically plastic characters may respond to multiple variables in their environment, but the evolutionary consequences of this phenomenon have rarely been addressed theoretically. We model the evolution of linear reaction norms in response to several correlated environmental variables, in a population undergoing stationary environmental fluctuations. At evolutionary equilibrium, the linear combination of environmental variables that acts as a developmental cue for the plastic trait is the multivariate best linear predictor of changes in the optimum. However, the reaction norm with respect to any single environmental variable may exhibit nonintuitive patterns. Apparently maladaptive, or hyperadaptive plasticity can evolve with respect to single environmental variables, and costs of plasticity may increase, rather than reduce, plasticity in response to some variables. We also find conditions for the evolution of an indirect environmental indicator that affects expression of a plastic phenotype, despite not influencing natural selection on it.     

The genetics of phenotypic plasticity. V. Evolution of reaction norm shape

We present a general quantitative genetic model for the evolution of reaction norms. This model goes beyond previous models by simultaneously permitting any shaped reaction norm and allowing for the imposition of genetic constraints. Earlier models are shown to be special cases of our general model; we discuss in detail models involving just two macroenvironments, linear reaction norms, and quadratic reaction norms. The model predicts that, for the case of a temporally varying environment, a population will converge on (1) the genotype with the maximum mean geometric fitness over all environments, (2) a linear reaction norm whose slope is proportional to the covariance between the environment of development and the environment of selection, and (3) a linear reaction norm even if nonlinear reaction norms are possible. An examination of experimental studies finds some limited support for these predictions. We discuss the limitations of our model and the need for more realistic gametic models and additional data on the genetic and developmental bases of plasticity.     

Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation

Adaptation to a sudden extreme change in environment, beyond the usual range of background environmental fluctuations, is analysed using a quantitative genetic model of phenotypic plasticity. Generations are discrete, with time lag τ between a critical period for environmental influence on individual development and natural selection on adult phenotypes. The optimum phenotype, and genotypic norms of reaction, are linear functions of the environment. Reaction norm elevation and slope (plasticity) vary among genotypes. Initially, in the average background environment, the character is canalized with minimum genetic and phenotypic variance, and no correlation between reaction norm elevation and slope. The optimal plasticity is proportional to the predictability of environmental fluctuations over time lag τ. During the first generation in the new environment the mean fitness suddenly drops and the mean phenotype jumps towards the new optimum phenotype by plasticity. Subsequent adaptation occurs in two phases. Rapid evolution of increased plasticity allows the mean phenotype to closely approach the new optimum. The new phenotype then undergoes slow genetic assimilation, with reduction in plasticity compensated by genetic evolution of reaction norm elevation in the original environment.     

THE EVOLUTION OF GENES IN BRANCHED METABOLIC PATHWAYS

Simulation models of the evolution of genes in a branched metabolic pathway subject to stabilizing selection on flux are described and analyzed. The models are based either on metabolic control theory (MCT), with the assumption that enzymes are far from saturation, or on Michaelis–Menten kinetics, which allows for saturation and near saturation. Several predictions emerge from the models: (1) flux control evolves to be concentrated at pathway branch points, including the first enzyme in the pathway. (2) When flux is far from its optimum, adaptive substitutions occur disproportionately often in branching enzymes. (3) When flux is near its optimum, adaptive substitutions occur disproportionately often in nonbranching enzymes. (4) Slightly deleterious substitutions occur disproportionately often in nonbranching enzymes. (5) In terms of both flux control and patterns of substitution, pathway branches are similar to those predicted for linear pathways. These predictions provide null hypotheses for empirical examination of the evolution of genes in metabolic pathways.     

The hitchhiker's guide to altruism: gene-culture coevolution,and the internalization of norms

An internal norm is a pattern of behavior enforced in part by internal sanctions, such as shame, guilt and loss of self-esteem, as opposed to purely external sanctions, such as material rewards and punishment. The ability to internalize norms is widespread among humans, although in some so-called "sociopaths", this capacity is diminished or lacking. Suppose there is one genetic locus that controls the capacity to internalize norms. This model shows that if an internal norm is fitness enhancing, then for plausible patterns of socialization, the allele for internalization of norms is evolutionarily stable. This framework can be used to model Herbert Simon's (1990) explanation of altruism, showing that altruistic norms can "hitchhike" on the general tendency of internal norms to be personally fitness-enhancing. A multi-level selection, gene-culture coevolution argument then explains why individually fitness-reducing internal norms are likely to be prosocial as opposed to socially harmful.     

Selection for distinct gene expression properties favours the evolution of mutational robustness in gene regulatory networks

Mutational robustness is a genotype's tendency to keep a phenotypic trait with little and few changes in the face of mutations. Mutational robustness is both ubiquitous and evolutionarily important as it affects in different ways the probability that new phenotypic variation arises. Understanding the origins of robustness is specially relevant for systems of development that are phylogenetically widespread and that construct phenotypic traits with a strong impact on fitness. Gene regulatory networks are examples of this class of systems. They comprise sets of genes that, through cross‐regulation, build the gene activity patterns that define cellular responses, different tissues or distinct cell types. Several empirical observations, such as a greater robustness of wild‐type phenotypes, suggest that stabilizing selection underlies the evolution of mutational robustness. However, the role of selection in the evolution of robustness is still under debate. Computer simulations of the dynamics and evolution of gene regulatory networks have shown that selection for any gene activity pattern that is steady and self‐sustaining is sufficient to promote the evolution of mutational robustness. Here, I generalize this scenario using a computational model to show that selection for different aspects of a gene activity phenotype increases mutational robustness. Mutational robustness evolves even when selection favours properties that conflict with the stationarity of a gene activity pattern. The results that I present support an important role for stabilizing selection in the evolution of robustness in gene regulatory networks.     

Divergence and ontogenetic coupling of larval behaviour and thermal reaction norms in three closely related butterflies

Genetic trade-offs such as between generalist–specialist strategies can be masked by changes in compensatory processes involving energy allocation and acquisition which regulation depends on the state of the individual and its ecological surroundings. Failure to account for such state dependence may thus lead to misconceptions about the trade-off structure and nature of constraints governing reaction norm evolution. Using three closely related butterflies, we first show that foraging behaviours differ between species and change remarkably throughout ontogeny causing corresponding differences in the thermal niches experienced by the foraging larvae. We further predicted that thermal reaction norms for larval growth rate would show state-dependent variation throughout development as a result of selection for optimizing feeding strategies in the respective foraging niches of young and old larvae. We found substantial developmental plasticity in reaction norms that was species-specific and reflected the different ontogenetic niche shifts. Any conclusions regarding constraints on performance curves or species-differentiation in thermal physiology depend on when reaction norms were measured. This demonstrates that standardized estimates at single points in development, or in general, allow variation in only one ecological dimension, may sometimes provide incomplete information on reaction norm constraints.     

Developmental canalization with no part of stabilizing selection

Referring the developmental canalization to stabilizing selection may be a bias that results from the ignorance of developmental mechanisms. Considering the morphological evolution of one-cell trichomes in Draba plants makes it clear that the transition from continuous variation in morphological traits to developmental creods occurs in the evolution of remote lineages of the genus irrespective of contribution to the net fitness. Morphological diversification of trichome branching is not under selection control, being a physical consequence of the trichome cell volume growth equilibrated by complication of the cell surface shape. At the start of evolution, the trichome development refers not to an individual trichome, but rather to repetitive trichome modules (branches), whose spatiotemporal order is arbitrary, except that some variants of branching depend on events that occur at earlier developmental stages more than others. Under selection fluctuating at random, or with no selection at all, fixing of these variants leads to the formation of trichome ontogeny, in which earlier developmental stages correspond to later stages of developmental evolution.     

Disruptive selection as a driver of evolutionary branching and caste evolution in social insects

Theory suggests that evolutionary branching via disruptive selection may be a relatively common and powerful force driving phenotypic divergence. Here, we extend this theory to social insects, which have novel social axes of phenotypic diversification. Our model, built around turtle ant (Cephalotes) biology, is used to explore whether disruptive selection can drive the evolutionary branching of divergent colony phenotypes that include a novel soldier caste. Soldier evolution is a recurrent theme in social insect diversification that is exemplified in the turtle ants. We show that phenotypic mutants can gain competitive advantages that induce disruptive selection and subsequent branching. A soldier caste does not generally appear before branching, but can evolve from subsequent competition. The soldier caste then evolves in association with specialized resource preferences that maximize defensive performance. Overall, our model indicates that resource specialization may occur in the absence of morphological specialization, but that when morphological specialization evolves, it is always in association with resource specialization. This evolutionary coupling of ecological and morphological specialization is consistent with recent empirical evidence, but contrary to predictions of classical caste theory. Our model provides a new theoretical understanding of the ecology of caste evolution that explicitly considers the process of adaptive phenotypic divergence and diversification.     

Social Norms of Cooperation in Small-Scale Societies

Indirect reciprocity, besides providing a convenient framework to address the evolution of moral systems, offers a simple and plausible explanation for the prevalence of cooperation among unrelated individuals. By helping someone, an individual may increase her/his reputation, which may change the pre-disposition of others to help her/him in the future. This, however, depends on what is reckoned as a good or a bad action, i.e., on the adopted social norm responsible for raising or damaging a reputation. In particular, it remains an open question which social norms are able to foster cooperation in small-scale societies, while enduring the wide plethora of stochastic affects inherent to finite populations. Here we address this problem by studying the stochastic dynamics of cooperation under distinct social norms, showing that the leading norms capable of promoting cooperation depend on the community size. However, only a single norm systematically leads to the highest cooperative standards in small communities. That simple norm dictates that only whoever cooperates with good individuals, and defects against bad ones, deserves a good reputation, a pattern that proves robust to errors, mutations and variations in the intensity of selection.     

Developmental constraints vs. variational properties: How pattern formation can help to understand evolution and development

This article suggests that apparent disagreements between the concept of developmental constraints and neo-Darwinian views on morphological evolution can disappear by using a different conceptualization of the interplay between development and selection. A theoretical framework based on current evolutionary and developmental biology and the concepts of variational properties, developmental patterns and developmental mechanisms is presented. In contrast with existing paradigms, the approach in this article is specifically developed to compare developmental mechanisms by the morphological variation they produce and the way in which their functioning can change due to genetic variation. A developmental mechanism is a gene network, which is able to produce patterns in space though the regulation of some cell behaviour (like signalling, mitosis, apoptosis, adhesion, etc.). The variational properties of a developmental mechanism are all the pattern transformations produced under different initial and environmental conditions or IS-mutations. IS-mutations are DNA changes that affect how two genes in a network interact, while T-mutations are mutations that affect the topology of the network itself. This article explains how this new framework allows predictions not only about how pattern formation affects variation, and thus phenotypic evolution, but also about how development evolves by replacement between pattern formation mechanisms. This article presents testable inferences about the evolution of the structure of development and the phenotype under different selective pressures. That is what kind of pattern formation mechanisms, in which relative temporal order, and which kind of phenotypic changes, are expected to be found in development.     

Evolution of sexual preferences in quantitative characters

An analysis of equilibria and dynamics of the means, variances, and covariances of female mating preference for a quantitative male secondary sexual character following a Gaussian model is presented. For many combinations of viability and sexual selection parameters the evolving Gaussian distribution of phenotypes can diverge. The results on the cases of convergence and their limiting forms suggest some reinterpretations of Fisher's "runaway" process of sexual selection. One possibility is to interpret Fisher's postulated "initial advantage not due to female preference" as a shift in viability selection where runaway evolution occurs if the mean preferred trait evolves beyond its new viability optimum (due to sexual selection). This definition is contrasted with situations in which the new viability optimum is undershot. The quantitative and qualitative conclusions differ from models that approximate genetic covariance evolution involving a constant covariance.     

Gene regulation,quantitative genetics and the evolution of reaction norms

Summary The ideas of phenotypic plasticity and of reaction norm are gaining prominence as important components of theories of phenotypic evolution. Our understanding of the role of phenotypic plasticity as an adaptation of organisms to variable environments will depend on (1) the form(s) of genetic and developmental control exerted on the shape of the reaction norm and (2) the nature of the constraints on the possible evolutionary trajectories in multiple environments. In this paper we identify two categories of genetic control of plasticity: allelic sensitivity and gene regulation. These correspond generally to two classes of response by the developmental system to environmental change: phenotypic modulation, in which plastic responses are a continuous and proportional function of environmental stimuli and developmental conversion, where responses tend to be not simply proportional to the stimuli. We propose that control of plasticity by regulatory actions has distinct advantages over simple allelic sensitivity: stability of phenotypic expression, capacity for anticipatory response and relaxation of constraints due to genetic correlations. We cite examples of the extensive molecular evidence for the existence of environmentally-cued gene regulation leading to developmental conversion. The results of quantitative genetic investigations on the genetics and evolution of plasticity, as well as the limits of current approaches are discussed. We suggest that evolution of reaction norms would be affected by the ecological context (i.e. spatial versus temporal variation, hard versus soft selection, and fine versus coarse environmental grain). We conclude by discussing some empirical approaches to address fundamental questions about plasticity evolution.