Promising directions in plant phenotypic plasticity

A research agenda for the next phase of plasticity studies calls for contributions from a diverse group of biologists, working both independently and collaboratively, to pursue four promising directions: examining dynamic, anatomical/architectural, and cross-generational plasticity along with simpler growth traits; carefully assessing the adaptive significance of those plasticity patterns; investigating the intricate transduction pathways that lead from environmental signal to phenotypic response; and considering the rich environmental context of natural systems. Progress in these areas will allow us to address broad and timely questions regarding the ecological and evolutionary significance of plasticity and the nature of phenotypic determination.     

Constant relative age and size at sex change for sequentially hermaphroditic fish

A general problem in evolutionary biology is that quantitative tests of theory usually require a detailed knowledge of the underlying trade-offs, which can be very hard to measure. Consequently, tests of theory are often constrained to be qualitative and not quantitative. A solution to this problem can arise when life histories are viewed in a dimensionless way. Recently, dimensionless theory has been developed to predict the size and age at which individuals should change sex. This theory predicts that the size at sex change/maximum size (L50/L(max)), and the age at sex change/age at first breeding (tau/alpha) should both be invariant. We found support for these two predictions across 52 species of fish. Fish change sex when they are 80% of their maximum body size, and 2.5 times their age at maturity. This invariant result holds despite a 60 and 25 fold difference across species in maximum size and age at sex change. These results suggest that, despite ignoring many biological complexities, relatively simple evolutionary theory is able to explain quantitatively at what point sex change occurs across fish species. Furthermore, our results suggest some very broad generalities in how male fitness varies with size and age across fish species with different mating systems.     

The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change

Species are the unit of analysis in many global change and conservation biology studies; however, species are not uniform entities but are composed of different, sometimes locally adapted, populations differing in plasticity. We examined how intraspecific variation in thermal niches and phenotypic plasticity will affect species distributions in a warming climate. We first developed a conceptual model linking plasticity and niche breadth, providing five alternative intraspecific scenarios that are consistent with existing literature. Secondly, we used ecological niche‐modeling techniques to quantify the impact of each intraspecific scenario on the distribution of a virtual species across a geographically realistic setting. Finally, we performed an analogous modeling exercise using real data on the climatic niches of different tree provenances. We show that when population differentiation is accounted for and dispersal is restricted, forecasts of species range shifts under climate change are even more pessimistic than those using the conventional assumption of homogeneously high plasticity across a species' range. Suitable population‐level data are not available for most species so identifying general patterns of population differentiation could fill this gap. However, the literature review revealed contrasting patterns among species, urging greater levels of integration among empirical, modeling and theoretical research on intraspecific phenotypic variation.     

Avoiding extinction under nonlinear environmental change: models of evolutionary rescue with plasticity

Rapid environmental changes are putting numerous species at risk of extinction. For migration-limited species, persistence depends on either phenotypic plasticity or evolutionary adaptation (evolutionary rescue). Current theory on evolutionary rescue typically assumes linear environmental change. Yet accelerating environmental change may pose a bigger threat. Here, we present a model of a species encountering an environment with accelerating or decelerating change, to which it can adapt through evolution or phenotypic plasticity (within-generational or transgenerational). We show that unless either form of plasticity is sufficiently strong or adaptive genetic variation is sufficiently plentiful, accelerating or decelerating environmental change increases extinction risk compared to linear environmental change for the same mean rate of environmental change.     

How stress selects for reversible phenotypic plasticity

Stress occurring in periods shorter than life span strongly selects for reversible phenotypic plasticity, for maximum reliability of stress indicating cues and for minimal response delays. The selective advantage of genotypes that are able to produce adaptive reversible plastic phenotypes is calculated by using the concept of environmental tolerance. Analytic expressions are given for optimal values of mode and breadth of tolerance functions for stress induced and non-induced phenotypes depending on (1) length of stress periods, (2) response delay for switching into the induced phenotype, (3) response delay for rebuilding the non-induced phenotype, (4) intensity of stress, i.e. mean value of the stress inducing environment, (5) coefficient of variation of the stress environment and (6) completeness of information available to the stressed organism. Adaptively reversible phenotypic plastic traits will most probably affect fitness in a way that can be described by simultaneous reversible plasticity in mode and breadth of tolerance functions.     

Phenotypic plasticity and divergence in gene expression

The extent to which phenotypic plasticity, or the ability of a single genotype to produce different phenotypes in different environments, impedes or promotes genetic divergence has been a matter of debate within evolutionary biology for many decades (see, for example, Ghalambor et al. 2007 ; Pfennig et al. 2010 ). Similarly, the role of evolution in shaping phenotypic plasticity remains poorly understood (Pigliucci 2005 ). In this issue of Molecular Ecology, Dayan et al. ( 2015 ) provide empirical data relevant to these questions by assessing the extent of plasticity and divergence in the expression levels of 2272 genes in muscle tissue from killifish (genus Fundulus) exposed to different temperatures. F. heteroclitus (Fig.  1 A) and F. grandis are minnows that inhabit estuarine marshes (Fig.  1 B) along the coasts of the Atlantic Ocean and Gulf of Mexico in North America. These habitats undergo large variations in temperature both daily and seasonally, and these fish are known to demonstrate substantial phenotypic plasticity in response to temperature change (e.g. Fangue et al. 2006 ). Furthermore, the range of F. heteroclitus spans a large latitudinal gradient of temperatures, such that northern populations experience temperatures that are on average ~10°C colder than do southern populations (Schulte 2007 ). By comparing gene expression patterns between populations of these fish from different thermal habitats held in the laboratory at three different temperatures, Dayan et al. ( 2015 ) address two important questions regarding the interacting effects of plasticity and evolution: (i) How does phenotypic plasticity affect adaptive divergence? and (ii) How does adaptive divergence affect plasticity?     

Gene expression plasticity evolves in response to colonization of freshwater lakes in threespine stickleback

Phenotypic plasticity is predicted to facilitate individual survival and/or evolve in response to novel environments. Plasticity that facilitates survival should both permit colonization and act as a buffer against further evolution, with contemporary and derived forms predicted to be similarly plastic for a suite of traits. On the other hand, given the importance of plasticity in maintaining internal homeostasis, derived populations that encounter greater environmental heterogeneity should evolve greater plasticity. We tested the evolutionary significance of phenotypic plasticity in coastal British Columbian postglacial populations of threespine stickleback (Gasterosteus aculeatus) that evolved under greater seasonal extremes in temperature after invading freshwater lakes from the sea. Two ancestral (contemporary marine) and two derived (contemporary freshwater) populations of stickleback were raised near their thermal tolerance extremes, 7 and 22 °C. Gene expression plasticity was estimated for more than 14 000 genes. Over five thousand genes were similarly plastic in marine and freshwater stickleback, but freshwater populations exhibited significantly more genes with plastic expression than marine populations. Furthermore, several of the loci shown to exhibit gene expression plasticity have been previously implicated in the adaptive evolution of freshwater populations, including a gene involved in mitochondrial regulation (PPARAa). Collectively, these data provide molecular evidence that highlights the importance of plasticity in colonization and adaptation to new environments.     

表型可塑性和局域适应在紫茎泽兰入侵不同海拔生境中的作用

紫茎泽兰是我国危害最严重的外来入侵物种之一,为探讨表型可塑性和局域适应在其入侵中的作用,在高、低海拔的两个样地内,测定了来自云南南部640～2450 m海拔范围的6个种源的紫茎泽兰种群的株高、冠宽、分枝数和高温半致死温度(HSLT).结果表明,在高海拔样地,各种群紫茎泽兰株高、冠宽、分枝数和HSLT(2130 m的哀牢山种群除外)均显著低于在低海拔样地,紫茎泽兰各种群的株高、冠宽和分枝数的可塑性指数(0.881～0.975)均较大,而HSLT的可塑性(0.052～0.200)较小.无论在高还是低海拔样地,紫茎泽兰的株高、冠宽和分枝数在种群间的差异均不显著,而HSLT在种群间的差异达极显著水平,表现出明显的遗传分化,但其在种群间的差异仍小于其在样地间的差异.在高海拔样地,紫茎泽兰各种群的分枝数与种源海拔呈显著正相关;在低海拔样地,紫茎泽兰的HSLT与种源海拔呈显著负相关,表现出明显的局域适应特征.表型可塑性和局域适应均与紫茎泽兰的入侵有关,但前者的作用可能更大.     

Adaptive phenotypic plasticity and local adaptation for temperature tolerance in freshwater zooplankton

Many organisms have geographical distributions extending from the tropics to near polar regions or can experience up to 30°C temperature variation within the lifespan of an individual. Two forms of evolutionary adaptation to such wide ranges in ambient temperatures are frequently discussed: local adaptation and phenotypic plasticity. The freshwater planktonic crustacean Daphnia magna, whose range extends from South Africa to near arctic sites, shows strong phenotypic and genotypic variation in response to temperature. In this study, we use D. magna clones from 22 populations (one clone per population) ranging from latitude 0° (Kenya) to 66° North (White Sea) to explore the contributions of phenotypic plasticity and local adaptation to high temperature tolerance. Temperature tolerance was studied as knockout time (time until immobilization, T_imm) at 37°C in clones acclimatized to either 20°C or 28°C. Acclimatization to 28°C strongly increased T_imm, testifying to adaptive phenotypic plasticity. At the same time, T_imm significantly correlated with average high temperature at the clones’ sites of origin, suggesting local adaptation. As earlier studies have found that haemoglobin expression contributes to temperature tolerance, we also quantified haemoglobin concentration in experimental animals and found that both acclimatization temperature (AccT) and temperature at the site of origin are positively correlated with haemoglobin concentration. Furthermore, Daphnia from warmer climates upregulate haemoglobin much more strongly in response to AccT, suggesting local adaptation for plasticity in haemoglobin expression. Our results show that both local adaptation and phenotypic plasticity contribute to temperature tolerance, and elucidate a possible role of haemoglobin in mediating these effects that differs along a cold–warm gradient.     

Epigenetics in natural animal populations

Phenotypic plasticity is an important mechanism for populations to buffer themselves from environmental change. While it has long been appreciated that natural populations possess genetic variation in the extent of plasticity, a surge of recent evidence suggests that epigenetic variation could also play an important role in shaping phenotypic responses. Compared with genetic variation, epigenetic variation is more likely to have higher spontaneous rates of mutation and a more sensitive reaction to environmental inputs. In our review, we first provide an overview of recent studies on epigenetically encoded thermal plasticity in animals to illustrate environmentally‐mediated epigenetic effects within and across generations. Second, we discuss the role of epigenetic effects during adaptation by exploring population epigenetics in natural animal populations. Finally, we evaluate the evolutionary potential of epigenetic variation depending on its autonomy from genetic variation and its transgenerational stability. Although many of the causal links between epigenetic variation and phenotypic plasticity remain elusive, new data has explored the role of epigenetic variation in facilitating evolution in natural populations. This recent progress in ecological epigenetics will be helpful for generating predictive models of the capacity of organisms to adapt to changing climates.     

Transgenerational plasticity mitigates the impact of global warming to offspring sex ratios

Global warming poses a threat to organisms with temperature‐dependent sex determination because it can affect operational sex ratios. Using a multigenerational experiment with a marine fish, we provide the first evidence that parents developing from early life at elevated temperatures can adjust their offspring gender through nongenetic and nonbehavioural means. However, this adjustment was not possible when parents reproduced, but did not develop, at elevated temperatures. Complete restoration of the offspring sex ratio occurred when parents developed at 1.5 °C above the present‐day average temperature for one generation. However, only partial improvement in the sex ratio occurred at 3.0 °C above average conditions, even after two generations, suggesting a limitation to transgenerational plasticity when developmental temperature is substantially increased. This study highlights the potential for transgenerational plasticity to ameliorate some impacts of climate change and that development from early life may be essential for expression of transgenerational plasticity in some traits.     

Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish

Divergent selection acting on several different traits that cause multidimensional shifts are supposed to promote speciation, but the outcome of this process is highly dependent on the balance between the strength of selection vs. gene flow. Here, we studied a pair of sister species of Lake Victoria cichlids at a location where they hybridize and tested the hypothesis that divergent selection acting on several traits can maintain phenotypic differentiation despite gene flow. To explore the possible role of selection we tested for correlations between phenotypes and environment and compared phenotypic divergence (P_ST) with that based on neutral markers (F_ST). We found indications for disruptive selection acting on male breeding colour and divergent selection acting on several morphological traits. By performing common garden experiments we also separated the environmental and heritable components of divergence and found evidence for phenotypic plasticity in some morphological traits contributing to species differences.     

Variation in the degree and costs of adaptive phenotypic plasticity among Rana temporaria populations

Adaptive phenotypic plasticity in the form of capacity to accelerate development as a response to pond drying risk is known from many amphibian species. However, very little is known about factors that might constrain the evolution of this type of plasticity, and few studies have explored to what degree plasticity might be constrained by trade-offs dictated by adaptation to different environmental conditions. We compared the ability of southern and northern Scandinavian common frog (Rana temporaria) larvae originating from 10 different populations to accelerate their development in response to simulated pond drying risk and the resulting costs in metamorphic size in a factorial laboratory experiment. We found that (i) northern larvae developed faster than the southern larvae in all treatments, (ii) a capacity to accelerate the response was present in all five southern and all five northern populations tested, but that the magnitude of the response was much larger (and less variable) in the southern than in the northern populations, and that (iii) significant plasticity costs in metamorphic size were present in the southern populations, the plastic genotypes having smaller metamorphic size in the absence of desiccation risk, but no evidence for plasticity costs was found in the northern populations. We suggest that the weaker response to pond drying risk in the northern populations is due to stronger selection on large metamorphic size as compared with southern populations. In other words, seasonal time constraints that have selected the northern larvae to be fast growing and developing, may also constrain their innate ability for adaptive phenotypic plasticity.     

Adaptive phenotypic plasticity in a clonal invader

Organisms featuring wide trait variability and occurring in a wide range of habitats, such as the ovoviviparous New Zealand freshwater snail Potamopyrgus antipodarum, are ideal models to study adaptation. Since the mid‐19th century, P. antipodarum, characterized by extremely variable shell morphology, has successfully invaded aquatic areas on four continents. Because these obligately and wholly asexual invasive populations harbor low genetic diversity compared to mixed sexual/asexual populations in the native range, we hypothesized that (1) this phenotypic variation in the invasive range might be adaptive with respect to colonization of novel habitats, and (2) that at least some of the variation might be caused by phenotypic plasticity. We surveyed 425 snails from 21 localities across northwest Europe to attempt to disentangle genetic and environmental effects on shell morphology. We analyzed brood size as proxy for fitness and shell geometric morphometrics, while controlling for genetic background. Our survey revealed 10 SNP genotypes nested into two mtDNA haplotypes and indicated that mainly lineage drove variation in shell shape but not size. Physicochemical parameters affected both shell shape and size and the interaction of these traits with brood size. In particular, stronger stream flow rates were associated with larger shells. Our measurements of brood size suggested that relatively larger slender snails with relatively large apertures were better adapted to strong flow than counterparts with broader shells and relatively small apertures. In conclusion, the apparent potential to modify shell morphology plays likely a key role in the invasive success of P. antipodarum; the two main components of shell morphology, namely shape and size, being differentially controlled, the former mainly genetically and the latter predominantly by phenotypic plasticity.     

生态因子及其交互作用对拟南芥(Arabidopsis thaliana)表型可塑性的影响

以拟南芥(Arabidopsis thaliana)两种基因型(ws-0和col-0)材料,采用复因子混合水平正交试验设计开展盆栽实验,研究了土壤盐分、土壤水分、光照强度、去叶处理等生态因子及其交互作用对受试植株18个表型特征的影响.结果表明生态因子对植物表型可塑性的影响是有针对性的:土壤水分主要影响植物体构件数目;土壤盐分主要影响生物量、角果数及种籽总数等直接反映植株适合度的表型特征;光照条件则主要影响植物的物候表型特征.植物体表型可塑性的方向随水分梯度的变化而发生改变.生态因子交互作用对植物表型可塑性的影响效果不是各因子独立作用的简单加和:对某个表型特征都有显著影响的两个生态因子其交互作用对该特征可能没有影响;反之,受两个生态因子交互作用影响显著的表型特征也可能不受它们的独立影响.在对生态因子交互作用作出响应时,col-0的9个特征表现出可塑性,而ws-0仅有4个表型是可塑的;同一基因型内彼此相关的表型特征在可塑性上也具一致性.抽苔时莲座叶数与角果平均籽粒数不受任何生态因子及其交互作用的影响,这两个表型作为数量特征而未表现出可塑性.     

Role of phenotypic plasticity and population differentiation in adaptation to novel environmental conditions

Species can adapt to new environmental conditions either through individual phenotypic plasticity, intraspecific genetic differentiation in adaptive traits, or both. Wild emmer wheat, Triticum dicoccoides, an annual grass with major distribution in Eastern Mediterranean region, is predicted to experience in the near future, as a result of global climate change, conditions more arid than in any part of the current species distribution. To understand the role of the above two means of adaptation, and the effect of population range position, we analyzed reaction norms, extent of plasticity, and phenotypic selection across two experimental environments of high and low water availability in two core and two peripheral populations of this species. We studied 12 quantitative traits, but focused primarily on the onset of reproduction and maternal investment, which are traits that are closely related to fitness and presumably involved in local adaptation in the studied species. We hypothesized that the population showing superior performance under novel environmental conditions will either be genetically differentiated in quantitative traits or exhibit higher phenotypic plasticity than the less successful populations. We found the core population K to be the most plastic in all three trait categories (phenology, reproductive traits, and fitness) and most successful among populations studied, in both experimental environments; at the same time, the core K population was clearly genetically differentiated from the two edge populations. Our results suggest that (1) two means of successful adaptation to new environmental conditions, phenotypic plasticity and adaptive genetic differentiation, are not mutually exclusive ways of achieving high adaptive ability; and (2) colonists from some core populations can be more successful in establishing beyond the current species range than colonists from the range extreme periphery with conditions seemingly closest to those in the new environment.     

The timescale of environmental fluctuations determines the competitive advantages of phenotypic plasticity and rapid evolution

Organisms can respond to fluctuating environments by phenotypic plasticity and rapid evolution, both occurring on similar timescales to the environmental fluctuations. Because each adaptation mechanism has been independently studied, the effects of different adaptation mechanisms on ecological dynamics are not well understood. Here, using mathematical modeling, we compared the advantages of phenotypic plasticity and rapid evolution under conditions where the environment fluctuated between two states on various timescales. The results indicate that the advantages of phenotypic plasticity under environmental fluctuations on different timescales depend on the cost and the speed of plasticity. Both the speed of plastic adaptation and the cost of plasticity affect competition results, while the quantitative effects of them vary depending on the timescales. When the environment fluctuates on short timescales, the two populations with evolution and plasticity coexist, although the population with evolution is dominant. On moderate timescales, the two populations also coexist; however, the population with plasticity becomes dominant. On long timescales, whether the population with phenotypic plasticity or evolution is more advantageous depended on the cost of plasticity. Moreover, our results indicate that the mechanisms resulting in the dominance of the plastic population over the population with evolution are different depending on the timescales of environmental fluctuations. Therefore, the timescales of environmental fluctuations deserve more attention if we are to better understand the detailed competition results underlying phenotypic variation.     

Snowshoe hares display limited phenotypic plasticity to mismatch in seasonal camouflage

As duration of snow cover decreases owing to climate change, species undergoing seasonal colour moults can become colour mismatched with their background. The immediate adaptive solution to this mismatch is phenotypic plasticity, either in phenology of seasonal colour moults or in behaviours that reduce mismatch or its consequences. We observed nearly 200 snowshoe hares across a wide range of snow conditions and two study sites in Montana, USA, and found minimal plasticity in response to mismatch between coat colour and background. We found that moult phenology varied between study sites, likely due to differences in photoperiod and climate, but was largely fixed within study sites with only minimal plasticity to snow conditions during the spring white-to-brown moult. We also found no evidence that hares modify their behaviour in response to colour mismatch. Hiding and fleeing behaviours and resting spot preference of hares were more affected by variables related to season, site and concealment by vegetation, than by colour mismatch. We conclude that plasticity in moult phenology and behaviours in snowshoe hares is insufficient for adaptation to camouflage mismatch, suggesting that any future adaptation to climate change will require natural selection on moult phenology or behaviour.