The genetics of phenotypic plasticity. XV. Genetic assimilation,the Baldwin effect,and evolutionary rescue

We used an individual‐based simulation model to examine the role of phenotypic plasticity on persistence and adaptation to two patterns of environmental variation, a single, abrupt step change and continual, linear change. Our model tested the assumptions and predictions of the theory of genetic assimilation, explored the evolutionary dynamics of the Baldwin effect, and provided expectations for the evolutionary response to climate change. We found that genetic assimilation as originally postulated is not likely to occur because the replacement of plasticity by fixed genetic effects takes much longer than the environment is likely to remain stable. On the other hand, trait plasticity as an enhancement to continual evolutionary change may be an important evolutionary mechanism as long as plasticity has little or no costs. Whether or not plasticity helps or hinders evolutionary rescue following a step change in the environment depends on whether plasticity is costly. For linear environmental change, noncostly plasticity always decreases extinction rates, while costly plasticity can create a fitness drag and increase the chance of extinction. Thus, with changing climates plasticity can enhance adaptation and prevent extinction under some conditions, but not others.     

Quantitative Assessment of the Importance of Phenotypic Plasticity in Adaptation to Climate Change in Wild Bird Populations

Predictions about the fate of species or populations under climate change scenarios typically neglect adaptive evolution and phenotypic plasticity, the two major mechanisms by which organisms can adapt to changing local conditions. As a consequence, we have little understanding of the scope for organisms to track changing environments by in situ adaptation. Here, we use a detailed individual-specific long-term population study of great tits (Parus major) breeding in Wytham Woods, Oxford, UK to parameterise a mechanistic model and thus directly estimate the rate of environmental change to which in situ adaptation is possible. Using the effect of changes in early spring temperature on temporal synchrony between birds and a critical food resource, we focus in particular on the contribution of phenotypic plasticity to population persistence. Despite using conservative estimates for evolutionary and reproductive potential, our results suggest little risk of population extinction under projected local temperature change; however, this conclusion relies heavily on the extent to which phenotypic plasticity tracks the changing environment. Extrapolating the model to a broad range of life histories in birds suggests that the importance of phenotypic plasticity for adjustment to projected rates of temperature change increases with slower life histories, owing to lower evolutionary potential. Understanding the determinants and constraints on phenotypic plasticity in natural populations is thus crucial for characterising the risks that rapidly changing environments pose for the persistence of such populations.     

Evolutionary and plastic rescue in multitrophic model communities

Under changing environmental conditions, intraspecific variation can potentially rescue populations from extinction. There are two principal sources of variation that may ultimately lead to population rescue: genetic diversity and phenotypic plasticity. We compared the potential for evolutionary rescue (through genetic diversity) and plastic rescue (through phenotypic plasticity) by analysing their differential ability to produce dynamical stability and persistence in model food webs. We also evaluated how rescue is affected by the trophic location of variation. We tested the following hypotheses: (i) plastic communities are more likely to exhibit stability and persistence than communities in which genetic diversity provides the same range of traits. (ii) Variation at the lowest trophic level promotes stability and persistence more than variation at higher levels. (iii) Communities with variation at two levels have greater probabilities of stability and persistence than communities with variation at only one level. We found that (i) plasticity promotes stability and persistence more than genetic diversity; (ii) variation at the second highest trophic level promotes stability and persistence more than variation at the autotroph level; and (iii) more than variation at two trophic levels. Our study shows that proper evaluation of the rescue potential of intraspecific variation critically depends on its origin and trophic location.     

Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations

Phenotypic plasticity provides means for adapting to environmental unpredictability. In terms of accelerated development in the face of pond-drying risk, phenotypic plasticity has been demonstrated in many amphibian species, but two issues of evolutionary interest remain unexplored. First, the heritable basis of plastic responses is poorly established. Second, it is not known whether interpopulational differences in capacity to respond to pond-drying risk exist, although such differences, when matched with differences in desiccation risk would provide strong evidence for local adaptation. We investigated sources of within- and among-population variation in plastic responses to simulated pond-drying risk (three desiccation treatments) in two Rana temporaria populations originating from contrasting environments: (1) high desiccation risk with weak seasonal time constraint (southern population); and (2) low desiccation risk with severe seasonal time constraint (northern population). The larvae originating from the environment with high desiccation risk responded adaptively to the fast decreasing water treatment by accelerating their development and metamorphosing earlier, but this was not the case in the larvae originating from the environment with low desiccation risk. In both populations, metamorphic size was smaller in the high-desiccation-risk treatment, but the effect was larger in the southern population. Significant additive genetic variation in development rate was found in the northern and was nearly significant in the southern population, but there was no evidence for genetic variation in plasticity for development rates in either of the populations. No genetic variation for plasticity was found either in size at metamorphosis or growth rate. All metamorphic traits were heritable, and additive genetic variances were generally somewhat higher in the southern population, although significantly so in only one trait. Dominance variances were also significant in three of four traits, but the populations did not differ. Maternal effects in metamorphic traits were generally weak in both populations. Within-environment phenotypic correlations between larval period and metamorphic size were positive and genetic correlations negative in both populations. These results suggest that adaptive phenotypic plasticity is not a species-specific fixed trait, but evolution of interpopulational differences in plastic responses are possible, although heritability of plasticity appears to be low. The lack of adaptive response to desiccation risk in northern larvae is consistent with the interpretation that selection imposed by shorter growing season has favored rapid development in north (approximately 8% faster development in north as compared to south) or a minimum metamorphic size at the expense of phenotypic plasticity.     

Phenotypic plasticity and selection in Drosophila life history evolution. 2. Diet,mates and the cost of reproduction

While it is commonplace for biologists to use the response to environmental manipulation as a guide to evolutionary responses to selection, the relationship between phenotypic plasticity and genetic change is not generally well-established. The life-histories of laboratory Drosophila populations are among the few experimental systems which simultaneously afford information on phenotypic plasticity and evolutionary trajectories. We employed a combination of two replicated selectively differentiated stocks (postponed aging stocks and their controls; 10 populations in total) and two different environmental manipulations (nutrition and mating) to explore the empirical relationship between phenotypic plasticity and evolutionary trajectories. While there are a number of parallels between the results obtained using these two approaches, there are important differences. In particular, as the detail of the biological characterization of either type of response increases, so their disparities multiply. Nonetheless, the combination of environmental manipulation with evolutionary divergence provides valuable information about the biological connections between life-history, caloric reserves, and reproductive physiology in Drososphila.     

WHEN DO ADAPTIVE PLASTICITY AND GENETIC EVOLUTION PREVENT EXTINCTION OF A DENSITY‐REGULATED POPULATION?

We study the dynamics of evolutionary recovery after an abrupt environmental shift in a density‐regulated population with evolving plasticity. Maladaptation to the new environment initially causes the population to decline, until adaptive phenotypic plasticity and genetic evolution restore positive population growth rate. We assume that selection on a quantitative trait is density‐independent and that the initial cost of plasticity is much lower than the benefit of the initial plastic response. The initial partially adaptive plasticity reduces the effective magnitude of the environmental shift, whereas evolution of plasticity increases the rate of adaptation. Both effects greatly facilitate population persistence. In contrast, density dependence of population growth always hinders persistence. With θ‐logistic population regulation, a lower value of θ produces a faster initial population decline and a higher extinction risk.     

Variation in developmental rates is not linked to environmental unpredictability in annual killifishes

Comparative evidence suggests that adaptive plasticity may evolve as a response to predictable environmental variation. However, less attention has been placed on unpredictable environmental variation, which is considered to affect evolutionary trajectories by increasing phenotypic variation (or bet hedging). Here, we examine the occurrence of bet hedging in egg developmental rates in seven species of annual killifish that originate from a gradient of variation in precipitation rates, under three treatment incubation temperatures (21, 23, and 25°C). In the wild, these species survive regular and seasonal habitat desiccation, as dormant eggs buried in the soil. At the onset of the rainy season, embryos must be sufficiently developed in order to hatch and complete their life cycle. We found substantial differences among species in both the mean and variation of egg development rates, as well as species‐specific plastic responses to incubation temperature. Yet, there was no clear relationship between variation in egg development time and variation in precipitation rate (environmental predictability). The exact cause of these differences therefore remains enigmatic, possibly depending on differences in other natural environmental conditions in addition to precipitation predictability. Hence, if species‐specific variances are adaptive, the relationship between development and variation in precipitation is complex and does not diverge in accordance with simple linear relationships.     

Phenotypic plasticity alone cannot explain climate‐induced change in avian migration timing

Recent climate change has been linked to shifts in the timing of life-cycle events in many organisms, but there is debate over the degree to which phenological changes are caused by evolved genetic responses of populations or by phenotypic plasticity of individuals. We estimated plasticity of spring arrival date in 27 species of bird that breed in the vicinity of an observatory in eastern North America. For 2441 individuals detected in multiple years, arrival occurred earlier during warm years, especially in species that migrate short distances. Phenotypic plasticity averaged −0.93 days °C⁻¹ ± 0.70 (95% CI). However, plasticity accounted for only 13–25% of the climate-induced trend in phenology observed over 46 years. Although our approach probably underestimates the full scope of plasticity, the data suggest that part of the response to environmental change has been caused by microevolution. The estimated evolutionary rates are plausible (0.016 haldanes).     

Ecological rescue of host-microbial systems under environmental change

Beneficial mutations can promote persistence via evolutionary rescue in species experiencing environmental change. However, in long-lived organisms, the pace of evolution is often too slow relative to that of environmental change for evolutionary rescue to occur. Using a spatially implicit metacommunity model, we demonstrate how interactions between slow-growing hosts and their fast-growing microbiomes can promote persistence under rapid environmental change. We show that microbial mutualists can rescue their hosts by allowing them to persist under deteriorating environmental conditions. This form of mutualist-mediated ecological rescue can be jeopardized by competitively dominant microbial cheaters, which can destabilize host population dynamics and promote the risk of stochastic extinction. However, when microbial diversity is high, (meta)community-level interactions among multiple microbial species can buffer the disruptive effect of cheaters and give rise to a more potent form of ecological rescue mediated by the entire microbiome that promotes the abundance, stability, and persistence of the host in the face of environmental change. Our results address two critical problems associated with the viability of rescue in macroorganisms: the temporal mismatch between rapid environmental change and slow organismal response and the potential disruption of rescue by microbial cheaters.     

Environmental determinants of population divergence in life‐history traits for an invasive species: climate,seasonality and natural enemies

Invasive species cope with novel environments through both phenotypic plasticity and evolutionary change. However, the environmental factors that cause evolutionary divergence in invasive species are poorly understood. We developed predictions for how different life‐history traits, and plasticity in those traits, may respond to environmental gradients in seasonal temperatures, season length and natural enemies. We then tested these predictions in four geographic populations of the invasive cabbage white butterfly (Pieris rapae) from North America. We examined the influence of two rearing temperatures (20 and 26.7 °C) on pupal mass, pupal development time, immune function and fecundity. As predicted, development time was shorter and immune function was greater in populations adapted to longer season length. Also, phenotypic plasticity in development time was greater in regions with shorter growing seasons. Populations differed significantly in mean and plasticity of body mass and fecundity, but these differences were not associated with seasonal temperatures or season length. Our study shows that some life‐history traits, such as development time and immune function, can evolve rapidly in response to latitudinal variation in season length and natural enemies, whereas others traits did not. Our results also indicate that phenotypic plasticity in development time can also diverge rapidly in response to environmental conditions for some traits.     

Plasticity paves the way in an adaptive radiation

Phenotypic plasticity has been hypothesized to play a central role in the evolution of phenotypic diversity across species (West‐Eberhard 2003 ). Through ‘genetic assimilation’, phenotypes that are initially environmentally induced within species become genetically fixed over evolutionary time. While genetic assimilation has been shown to occur in both the laboratory and the field (Waddington 1953 ; Aubret & Shine 2009 ), it remains to be shown whether it can account for broad patterns of phenotypic diversity across entire adaptive radiations. Furthermore, our ignorance of the underlying molecular mechanisms has hampered our ability to incorporate phenotypic plasticity into models of evolutionary processes. In this issue of Molecular Ecology, Parsons et al. ( 2016 ) take a significant step in filling these conceptual gaps making use of cichlid fishes as a powerful study system. Cichlid jaw and skull morphology show adaptive, plastic changes in response to early dietary experiences (Fig. 1). In this research, Parsons et al. ( 2016 ) first show that the direction of phenotypic plasticity aligns with the major axis of phenotypic divergence across species. They then dissect the underlying genetic architecture of this plasticity, showing that it is specific to the developmental environment and implicating the patched locus in genetic assimilation (i.e. a reduction in the environmental sensitivity of that locus in the derived species).     

Trait plasticity in species interactions: a driving force of community dynamics

Evolutionary community ecology is an emerging field of study that includes evolutionary principles such as individual trait variation and plasticity of traits to provide a more mechanistic insight as to how species diversity is maintained and community processes are shaped across time and space. In this review we explore phenotypic plasticity in functional traits and its consequences at the community level. We argue that resource requirement and resource uptake are plastic traits that can alter fundamental and realised niches of species in the community if environmental conditions change. We conceptually add to niche models by including phenotypic plasticity in traits involved in resource allocation under stress. Two qualitative predictions that we derive are: (1) plasticity in resource requirement induced by availability of resources enlarges the fundamental niche of species and causes a reduction of vacant niches for other species and (2) plasticity in the proportional resource uptake results in expansion of the realized niche, causing a reduction in the possibility for coexistence with other species. We illustrate these predictions with data on the competitive impact of invasive species. Furthermore, we review the quickly increasing number of empirical studies on evolutionary community ecology and demonstrate the impact of phenotypic plasticity on community composition. Among others, we give examples that show that differences in the level of phenotypic plasticity can disrupt species interactions when environmental conditions change, due to effects on realized niches. Finally, we indicate several promising directions for future phenotypic plasticity research in a community context. We need an integrative, trait-based approach that has its roots in community and evolutionary ecology in order to face fast changing environmental conditions such as global warming and urbanization that pose ecological as well as evolutionary challenges.     

植物的表型可塑性、异速生长及其入侵能力

表型可塑性是指同一个基因型对不同环境响应产生不同表型的特性,特定性状的可塑性本身可以遗传,也可以接受选择而发生进化。植物个体的异速生长是指生物体某一特征的相对生长速率不等于第二种特征的相对生长速率的特性,该特性是由物种的遗传性决定的一种固定特征,植物往往朝着最佳的异速生长曲线进化。植物特定基因型在不同环境下,诸如生物量分配和种群几何学上的一些表型差异,既可由异速生长造成,也可由表型可塑性造成。植物本身的异速生长是一种"外观可塑性",而异速生长曲线的改变才是真正的可塑性。植物的表型可塑性、异速生长对于入侵植物的适应具有重要意义。干扰等异质性生境下表型可塑性成为物种生存扩散的有利性状,表型可塑性强的物种更有可能成为广布种。植物本身的异速生长特性或其异速生长曲线的改变都能影响其入侵能力。     

EXPERIMENTAL EVOLUTION MEETS MARINE PHYTOPLANKTON

Our perspective highlights potentially important links between disparate fields—biological oceanography, climate change research, and experimental evolutionary biology. We focus on one important functional group—photoautotrophic microbes (phytoplankton), which are responsible for ～50% of global primary productivity. Global climate change currently results in the simultaneous change of several conditions such as warming, acidification, and nutrient supply. It thus has the potential to dramatically change phytoplankton physiology, community composition, and may result in adaptive evolution. Although their large population sizes, standing genetic variation, and rapid turnover time should promote swift evolutionary change, oceanographers have focussed on describing patterns of present day physiological differentiation rather than measure potential adaptation in evolution experiments, the only direct way to address whether and at which rate phytoplankton species will adapt to environmental change. Important open questions are (1) is adaptation limited by existing genetic variation or fundamental constraints? (2) Will complex ecological settings such as gradual versus abrupt environmental change influence adaptation processes? (3) How will increasing environmental variability affect the evolution of phenotypic plasticity patterns? Because marine phytoplankton species display rapid acclimation capacity (phenotypic buffering), a systematic study of reaction norms renders them particularly interesting to the evolutionary biology research community.     

Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature‐induced variation

Many animal lineages exhibit allometry in sexual size dimorphism (SSD), known as ‘Rensch’s rule’. When applied to the interspecific level, this rule states that males are more evolutionary plastic in body size than females and that male‐biased SSD increases with body size. One of the explanations for the occurrence of Rensch’s rule is the differential‐plasticity hypothesis assuming that higher evolutionary plasticity in males is a consequence of larger sensitivity of male growth to environmental cues. We have confirmed the pattern consistent with Rensch’s rule among species of the gecko genus Paroedura and followed the ontogeny of SSD at three constant temperatures in a male‐larger species (Paroedura picta). In this species, males exhibited larger temperature‐induced phenotypic plasticity in final body size than females, and body size and SSD correlated across temperatures. This result supports the differential‐plasticity hypothesis and points to the role phenotypic plasticity plays in generating of evolutionary novelties.     

The genetics of phenotypic plasticity. XI. Joint evolution of plasticity and dispersal rate

In a spatially heterogeneous environment, the rate at which individuals move among habitats affects whether selection favors phenotypic plasticity or genetic differentiation, with high dispersal rates favoring trait plasticity. Until now, in theoretical explorations of plasticity evolution, dispersal rate has been treated as a fixed, albeit probabilistic, characteristic of a population, raising the question of what happens when the propensity to disperse and trait plasticity are allowed to evolve jointly. We examined the effects of their joint evolution on selection for plasticity using an individual-based computer simulation model. In the model, the environment consisted of a linear gradient of 50 demes with dispersal occurring either before or after selection. Individuals consisted of loci whose phenotypic expression either are affected by the environment (plastic) or are not affected (nonplastic), plus a locus determining the propensity to disperse. When dispersal rate and trait plasticity evolve jointly, the system tends to dichotomous outcomes of either high trait plasticity and high dispersal, or low trait plasticity and low dispersal. The outcome strongly depended on starting conditions, with high trait plasticity and dispersal favored when the system started at high values for either trait plasticity or dispersal rate (or both). Adding a cost of plasticity tended to drive the system to genetic differentiation, although this effect also depended on initial conditions. Genetic linkage between trait plasticity loci and dispersal loci further enhanced this strong dichotomy in evolutionary outcomes. All of these effects depended on organismal life history pattern, and in particular whether selection occurred before or after dispersal. These results can explain why adaptive trait plasticity is less common than might be expected.     

EVOLUTION OF PHENOTYPE–ENVIRONMENT ASSOCIATIONS BY GENETIC RESPONSES TO SELECTION AND PHENOTYPIC PLASTICITY IN A TEMPORALLY AUTOCORRELATED ENVIRONMENT

Covariation between population‐mean phenotypes and environmental variables, sometimes termed a “phenotype–environment association” (PEA), can result from phenotypic plasticity, genetic responses to natural selection, or both. PEAs can potentially provide information on the evolutionary dynamics of a particular set of populations, but this requires a full theoretical characterization of PEAs and their evolution. Here, we derive formulas for the expected PEA in a temporally fluctuating environment for a quantitative trait with a linear reaction norm. We compare several biologically relevant scenarios, including constant versus evolving plasticity, and the situation in which an environment affects both development and selection but at different time periods. We find that PEAs are determined not only by biological factors (e.g., magnitude of plasticity, genetic variation), but also environmental factors, such as the association between the environments of development and of selection, and in some cases the level of temporal autocorrelation. We also describe how a PEA can be used to estimate the relationship between an optimum phenotype and an environmental variable (i.e., the environmental sensitivity of selection), an important parameter for determining the extinction risk of populations experiencing environmental change. We illustrate this ability using published data on the predator‐induced morphological responses of tadpoles to predation risk.     

Selection on heritable seasonal phenotypic plasticity of body mass

The ability to cope with environmental change is fundamental to a species' evolution. Organisms can respond to seasonal environmental variation through phenotypic plasticity. The substantial plasticity in body mass of temperate species has often been considered a simple consequence of change in environmental quality, but could also have evolved as an adaptation to seasonality. We investigated the genetic basis of, and selection acting on, seasonal plasticity in body mass for wild bighorn sheep ewes (Ovis canadensis) at Ram Mountain, Alberta, under two contrasting environmental conditions. Heritability of plasticity, estimated as mass-specific summer and winter mass changes, was low but significant. The additive genetic variance component of relative summer mass change was greater under good environmental conditions (characterized by a population increase and high juvenile survival) than under poor conditions (population decrease and low juvenile survival). Additive genetic variance of relative winter mass change appeared independent of environmental conditions. We found evidence of selection on summer (relative) and winter (relative and absolute) mass change. For a given mass, more plastic individuals (with greater seasonal mass changes) achieve greater fitness through reproduction in the following year. However, genetic correlations between mass parameters were positive. Our study supports the hypothesis that seasonal plasticity in body mass in vertebrates is an adaptation that evolved under natural selection to cope with environmental variation but genetic correlations with other traits might limit its evolutionary potential.     

PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION

The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation.