Physiological Mechanisms and the Evolution of Plasticity

Adaptive Phenotypic Plasticity: Target or By-Product of Selection in a Variable Environment?

Phenotypic plasticity may evolve rapidly, enabling a population’s persistence in the face of sudden environmental change. Rapid evolution can occur when there is considerable genetic polymorphism at selected loci. We propose that balancing selection could be one of the mechanisms that sustain such polymorphism for plasticity. We use stochastic Monte Carlo simulations and deterministic analysis to investigate the evolution of a plasticity modifier locus in structured populations inhabiting favorable and adverse environments, i.e. patchy habitats. We survey a wide range of parameters including selective pressures on a target (structural) locus, plasticity effects, population sizes, and migration patterns between demes including periodic or continuous bidirectional and source-sink dynamics. We find that polymorphism in phenotypic plasticity can be maintained under a wide range of environmental scenarios in both favorable and adverse environments due to the balancing effect of population structure in patchy habitats. This effect offers a new plausible explanation for the rapid evolution of plasticity in nature: Phenotypic plasticity may rapidly evolve from genetic variation maintained by balancing selection if the population has experienced immigration from populations under different selection regimes.

Evidence of selection on phenotypic plasticity and cost of plasticity in response to host-feeding sources in the major Chagas disease vector Triatoma infestans

Species that compete for the same resource may undergo ecological character displacement (CD), where the phenotype of each species evolves to deviate from its optimum in the absence of competition. As natural habitats are rarely static, interspecific competition is likely to occur in environments that fluctuate over time. Such environmental fluctuations can in turn cause the evolution of phenotypic plasticity for traits mediating the competition. However, the interplay of environmental fluctuations, evolution of plasticity, and character displacement, has been little investigated. We use a quantitative genetic model to study theoretically how a randomly fluctuating environment and evolution of plasticity influence the outcome of ecological CD between 2 competing species. We show that environmental fluctuations make the conditions for CD more stringent, requiring stronger competitive selection relative to stabilizing selection. This occurs because environmental fluctuations reduce the average population size and thereby competition intensity. Evolving plasticity can restore CD by buffering the impact of environmental fluctuations through phenotypic tracking, to a degree that depends on environmental predictability. Somewhat paradoxically, competition that favors phenotypic divergence among species can cause convergence in plasticity, when this reduces the load caused by fluctuations in phenotypic divergence. Our results shed light on how competition and plasticity influence the evolution of the fundamental niche in a fluctuating environment.

This theme issue pursues an exploration of the potential of taking into account the environmental sensitivity of development to explaining the evolution of metazoan life cycles, with special focus on complex life cycles and the role of developmental plasticity. The evolution of switches between alternative phenotypes as a response to different environmental cues and the evolution of the control of the temporal expression of alternative phenotypes within an organism's life cycle are here treated together as different dimensions of the complex relationships between genotype and phenotype, fostering the emergence of a more general and comprehensive picture of phenotypic evolution through a quite diverse sample of case studies. This introductory article reviews fundamental facts and concepts about phenotypic plasticity, adopting the most authoritative terminology in use in the current literature. The main topics are types and components of phenotypic variation, the evolution of organismal traits through plasticity, the origin and evolution of phenotypic plasticity and its adaptive value.

Chapter 18 - The Genomics of Cladoceran Physiology

Our understanding of the development and evolution of phenotypic plasticity has evolved in the 30 years since the first Dahlem conference on development and evolution. The focus of this review is on the developmental mechanisms that produce alternative and conditional phenotypes in response to environmental signals. The role of environment is a critical factor in evolution, yet environment is almost universally ignored in developmental biology. The effects of environment are most clearly seen in postembryonic development, where the mechanisms by which environmental signals alter developmental trajectories are increasingly well understood. The outcome of altered developmental pathways is what we recognize as phenotypic plasticity. This chapter shows that the developmental mechanisms that produce phenotypic plasticity are diverse and that control resides largely at the physiological level, often via developmental hormones that switch between alternative developmental fates in response to environmental signals. In conclusion this chapters shows how robustness and homeostatic mechanisms are they key to understanding the evolution of conditional traits.

The environmental variables hypothesized to cause behavioral adaptation are distributed across a wide array of spatial scales, from local variation in factors such as food sources and territorial encounters to regional or continental variation in factors such as seasonality and the presence of predators. Geographic variation in behavior, the topic of this book, is just one of the potential evolutionary responses to environmental variation. Because behavioral divergence among populations generated by disparate natural selection can be counterbalanced by the homogenizing influence of gene flow, adaptive geographic variation can evolve only if the spatial scale of variation in natural selection is greater than the scale of gene flow (Endler 1977, Slatkin 1978). If geographic variation does not evolve because the spatial scale of selection is smaller than the scale of gene flow, populations may instead evolve adaptive phenotypic plasticity (Bradshaw 1965); the expression, by a single genotype, of different fitness-enhancing phenotypes in different environments. Because the same evolutionary processes operating on different spatial scales can generate behavioral geographic variation, behavioral phenotypic plasticity, or geographic variation in phenotypic plasticity, I devote this chapter to development of a hierarchical perspective tor studying environmental variation and behavioral evolution. This perspective emphasizes the shared evolutionary processes and research methodologies common to different levels of spatial variation, such as the balance of gene flow, natural selection, and genetic drift, the relationship between environmental patch size and local adaptation, and the effects of historical contingencies and genetic constraints on behavioral adaptation and phenotypic plasticity. In what follows, I review behavioral research in two unrelated taxa to illustrate the range of possible evolutionary responses to different patterns of environmental variation. First, I discuss different spatial scales of adaptation in the climbing behavior of deer mice (Peromyscus maniculatus) and provide a hierarchical analysis of the effects of natural selection, genetic drift, and gene flow. Second, I discuss diet-induced phenotypic plasticity in the feeding behavior of acridid grasshoppers (Melanoplus femurrubrum and M. sanguinipes) and the evolution of behavioral norms of reaction in response to local spatial and temporal variation in plant environments.

The evolution of language has been the subject of much debate and speculation. It is difficult to study in a scientific manner and remains an open research question. This paper proposes an integrated computational framework for investigating possible scenarios of genetic and cultural evolution of language. Specifically, our framework aims to capture cultural evolution to allow for investigation phylogenetic dynamics of language, and at the same time to capture genetic evolution of phenotypic plasticity to allow for investigation of the role of the Baldwin effect in language evolution, while keeping the framework as simple as possible. In our evolutionary experiments and analysis, we discovered a coevolutionary scenario involving biological evolution of phenotypic plasticity, and a cyclic coevolutionary dynamic between genetic and cultural evolution, mediated by phenotypic plasticity.

Environmental variation in temperature can have dramatic effects on plant morphology, phenology, and fitness, and for this reason it is important to understand the evolutionary dynamics of phenotypic plasticity in response to temperature. We investigated constraints on the evolution of phenotypic plasticity in response to a temperature gradient in the model plant Arabidopsis thaliana by applying modern analytical tools to the classic data of Westerman & Lawrence (1970). We found significant evidence for two types of constraints. First, we detected numerous significant genetic correlations between plastic responses to temperature and the mean value of a trait across all environments, which differed qualitatively in pattern between the set of ecotypes and the set of mutant lines in the original sample. Secondly, we detected significant costs of flowering time plasticity in two of the three experimental environments, and a net pattern of selection against flowering time plasticity in the experiment overall. Thus, when explored with contemporary methods, the prescient work of Westerman & Lawrence (1970) provides new insights about evolutionary constraints on the evolution of plasticity.

Phenotypic plasticity allows organisms to improve the match between their phenotype and heterogeneous environments. Theoretical models have argued that costs of maintaining the sensory and response machinery necessary for adaptive phenotypic plasticity are important determinants to the evolution of plasticity. Despite recurrent arguments invoking putative metabolic costs associated with maintenance of cellular machinery, no studies have yet attempted to quantify it from a molecular standpoint. Here we experimentally examine physiological differences across genotypes (sibships) of spadefoot toad larvae with different degrees of plasticity in response to predator cues. We observed marked differences across sibships in developmental, growth and morphological responses to predators, and tested whether increased plasticity was associated with oxidative stress or immune suppression. We observed that more plastic sibships experienced higher antioxidant enzymatic activity when reared in the absence of predator cues, i.e. not expressing their plastic responses. The degree of plasticity was also associated with higher lipid peroxidation and slightly greater granulocyte‐to‐lymphocyte ratio. Higher antioxidant activity in highly plastic sibships suggests that maintenance of phenotypic plasticity may be linked to energy demanding metabolic processes. Our findings suggest that having the potential to produce plastic responses may incur oxidative and immunological costs. In the long term, such maintenance costs may erode individual fitness and even constrain the evolution of plasticity. To our knowledge, this is the first empirical evidence indicating the existence of a physiological cost to the maintenance of phenotypic plasticity.

Migrant species express wide varieties of movement strategies that closely mirror patterns of resource distribution. Resources can vary predictably in space and time (e.g., seasonal peaks of productivity in temperate regions) or can be unpredictable in one or both dimensions. Evolution of migration strategies and the underlying physiological and behavioral mechanisms are therefore diverse, but similarities have been noted. To understand how migrants respond to environmental cues, we focus on species that represent extremes along a continuum between obligate versus facultative migratory behavior and address the physiological mechanisms regulating these movements. Obligate migrants, which travel on highly predictable schedules, generally rely on the annual change in daylength and circannual rhythms to initiate the vernal and, where known, the fall phases of migration. Facultative species may show similar seasonal preparations in cases where resources are temporally predictable, but appear to rely more heavily upon local supplementary cues in the environment to initiate migrations. In general, the physiological response mechanisms to environmental cues that coordinate migratory movements include perception of the environmental cue and transduction to neuroendocrine and endocrine systems. Clearly, there are huge gaps in our knowledge in this area, but published studies of each of the migratory types suggest striking parallels. Based on a comparison of the physiological aspects of the divergent migratory patterns, we emphasize that the migratory types are not completely distinct. Instead, the differences of migration patterns and responsiveness to cues reflect differences in the relative contributions of common physiological mechanisms that underly the control of movements. A more complete understanding of migratory physiology requires continued descriptive studies, particularly in a greater diversity of model systems, in addition to experimental methods that utilize innovative tracking technology as well as behavioral and physiological innovations to draw attention to different levels of organization. Comprehending the physiological mechanisms underlying migratory patterns will be vital for knowing how migrants respond to current environmental cues and anticipating their reactions to future conditions.

1 Phenotypic plasticity has long been suggested to facilitate biological invasions where a general purpose genotype or ‘Jack-of-all-trades’ strategy could facilitate invasion should native species be, on average, more specialized. Current understanding of the importance of phenotypic plasticity is limited by methodological difficulties yet glasshouse experiments, paralleling those used in evolutionary biology, are increasingly being used to assess whether invasive species have high phenotypic plasticity or not. Unfortunately, these studies have several major limitations. 2 In general, glasshouse experiments have quantified relatively labile means of expressing phenotypes, such as plant biomass, rather than changes in plant development. As some environments favour plant growth and reproduction more than others, simply quantifying allometric or physiological responses relating to differential plant growth may not reveal much about phenotypic plasticity. 3 Plasticity is often a comparative rather than an absolute measure. A range of comparators have been used, for example, unrelated natives, congeneric natives, other congeneric aliens or conspecifics from the source region. Thus, unlike many life-history traits used in analyses of invasion, phenotypic plasticity is strongly context-dependent and limits comparison across different studies. 4 Phenotypic plasticity is assumed to lead to a greater breadth of environmental conditions across which a species can maintain positive population growth and increase the likelihood of invasiveness. Yet, most studies examine only a partial subset of the full environmental range experienced by the species. If the reaction norm of a target species and its comparator vary independently across an environmental gradient, this partial approach can present different interpretations of phenotypic plasticity. 5 Rather than simply quantifying greater phenotypic plasticity in invasive species, research questions should be directed at better understanding its role in the geographic distribution, successful colonization, population persistence and/or high local abundance of invasive species in the introduced range. These issues require integrated measures of plant performance rather than crude differences in individual traits across an environmental gradient. As yet, there is only limited appreciation of the role of phenotypic plasticity in any one of these areas and there is a need to extend studies beyond glasshouse experiments.

Phenotypic plasticity is a common defensive strategy in species experiencing variable predation risk, such as habitat generalists. Larvae of generalist dragonflies can elongate their abdominal spines in environments with fish, but long spines render larvae susceptible to invertebrate predators. Long-spined specialists adapted to fish-heavy habitats are not expected to have phenotypic plasticity in this defence trait, but no empirical studies have been undertaken. Moreover, in comparison to prey responding to multiple predators that induce similar phenotypes, relatively little is known regarding how species react to combinations of predators that favour opposing traits. We examined plasticity of larval dragonfly Sympetrum depressiusculum, a long-spined habitat specialist. In a rearing experiment, larvae were exposed to four environments: (i) no predator control, (ii) fish cues (Carassius auratus), (iii) invertebrate cues (Anax imperator), as well as (iv) a combination of (ii) and (iii). Compared with the control, fish but not invertebrate cues resulted in longer spines for two (one lateral, one dorsal) of the six spines measured. Interestingly, the combined-cue treatment led to the elongation of all four dorsal spines compared with the fish treatment alone, whereas lateral spines showed no response. Our experiment provided evidence of morphological plasticity in a long-spined specialist dragonfly. We showed that nearly all spines can elongate, but also react differently under specific predator settings. Therefore, while spine plasticity evolved in direct response to a single predator type (fish), plasticity was maintained against invertebrate predators as long as fish were also present. Selective spine induction under the combined condition suggests that S. depressiusculum can successfully survive in environments with both predators. Therefore, phenotypic plasticity may be an effective strategy for habitat generalists and specialists. Although more studies are necessary to fully understand how selection shapes the evolution of phenotypic plasticity, we demonstrated that in dragonflies, presence or absence of a specific predator is not the only factor that determines plastic defence responses.

Will Roe Deer Persist in a Warmer World?