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.     

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.     

Population differences in host use by a seed-beetle: local adaptation, phenotypic plasticity and maternal effects

For insects that develop inside discrete hosts, both host size and host quality constrain offspring growth, influencing the evolution of body size and life history traits. Using a two-generation common garden experiment, we quantified the contribution of maternal and rearing hosts to differences in growth and life history traits between populations of the seed-feeding beetle Stator limbatus that use a large-seeded host, Acacia greggii, and a small-seeded host, Pseudosamanea guachapele. Populations differed genetically for all traits when beetles were raised in a common garden. Contrary to expectations from the local adaptation hypothesis, beetles from all populations were larger, developed faster and had higher survivorship when reared on seeds of A. greggii (the larger host), irrespective of their native host. We observed two host plant-mediated maternal effects: offspring matured sooner, regardless of their rearing host, when their mothers were reared on P. guachapele (this was not caused by an effect of rearing host on egg size), and females laid larger eggs on P. guachapele. This is the first study to document plasticity by S. limbatus in response to P. guachapele, suggesting that plasticity is an ancestral trait in S. limbatus that likely plays an important role in diet expansion. Although differences between populations in growth and life history traits are likely adaptations to their host plants, host-associated maternal effects, partly mediated by maternal egg size plasticity, influence growth and life history traits and likely play an important role in the evolution of the breadth of S. limbatus’ diet. More generally, phenotypic plasticity mediates the fitness consequences of using novel hosts, likely facilitating colonization of new hosts, but also buffering herbivores from selection post-colonization. Plasticity in response to novel versus normal hosts varied among our study populations such that disentangling the historical role of plasticity in mediating diet evolution requires the consideration of evolutionary history.     

The importance of phenotypic plasticity and local adaptation in driving intraspecific variability in thermal niches of marine macrophytes

Climate change is driving the redistribution of species at a global scale and documenting and predicting species' responses to warming is a principal focus of contemporary ecology. When interpreting and predicting their responses to warming, species are generally treated as single homogenous physiological units. However, local adaptation and phenotypic plasticity can result in intraspecific differences in thermal niche. Therefore, population loss may also not only occur from trailing edges. In species with low dispersal capacity this will have profound impacts for the species as a whole, as local population loss will not be offset by immigration of warm tolerant individuals. Recent evidence from terrestrial forests has shown that incorporation of intraspecific variation in thermal niche is vital to accurately predicting species responses to warming. However, marine macrophytes (i.e. seagrasses and seaweeds) that form some of the world's most productive and diverse ecosystems have not been examined in the same context. We conducted a literature review to determine how common intraspecific variation in thermal physiology is in marine macrophytes. We find that 90% of studies identified (n = 42) found clear differences in thermal niche between geographically separated populations. Therefore, non‐trailing edge populations may also be vulnerable to future warming trends and given their limited dispersal capacity, such population loss may not be offset by immigration. We also explore how next generation sequencing (NGS) is allowing unprecedented mechanistic insight into plasticity and adaptation. We conclude that in the ‘genomic era’ it may be possible to link understanding of plasticity and adaptation at the genetic level through to changes in populations providing novel insights on the redistribution of populations under future climate change.     

A history of phenotypic plasticity accelerates adaptation to a new environment

Can a history of phenotypic plasticity increase the rate of adaptation to a new environment? Theory suggests it can be through two different mechanisms. Phenotypically plastic organisms can adapt rapidly to new environments through genetic assimilation, or the fluctuating environments that result in phenotypic plasticity can produce evolvable genetic architectures. In this article, I studied a model of a gene regulatory network that determined a phenotypic character in one population selected for phenotypic plasticity and a second population in a constant environment. A history of phenotypic plasticity increased the rate of adaptation in a new environment, but the amount of this increase was dependent on the strength of selection in the original environment. Phenotypic variance in the original environment predicted the adaptive capacity of the trait within, but not between, plastic and nonplastic populations. These results have implications for invasive species and ecological studies of rapid adaptation.     

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.     

Testing the role of phenotypic plasticity for local adaptation: growth and development in time-constrained Rana temporaria populations

Phenotypic plasticity can be important for local adaptation, because it enables individuals to survive in a novel environment until genetic changes have been accumulated by genetic accommodation. By analysing the relationship between development rate and growth rate, it can be determined whether plasticity in life-history traits is caused by changed physiology or behaviour. We extended this to examine whether plasticity had been aiding local adaptation, by investigating whether the plastic response had been fixed in locally adapted populations. Tadpoles from island populations of Rana temporaria, locally adapted to different pool-drying regimes, were monitored in a common garden. Individual differences in development rate were caused by different foraging efficiency. However, developmental plasticity was physiologically mediated by trading off growth against development rate. Surprisingly, plasticity has not aided local adaptation to time-stressed environments, because local adaptation was not caused by genetic assimilation but on selection on the standing genetic variation in development time.     

The contribution of phenotypic plasticity to adaptation in Lacerta vivipara

Correlation between intraspecific phenotypic variability and variation of environmental conditions could reflect adaptation. Different phenotypes may result from differential expression of a genotype in different environments (phenotypic plasticity) or from expression of different genotypes (genetic diversity). Populations of Lacerta vivipara exhibit larger adult body length, lower age at maturity, higher fecundity, and smaller neonatal size in humid habitats compared to dry habitats. We conducted reciprocal transplants of juvenile L. vivipara to test for the genetic or plastic origin of this variation. We captured gravid females from four populations that differed in the relative humidity of their habitats, and during the last 2 to 4 weeks of gestation, we manipulated heat and water availability under laboratory conditions. Juveniles were released into the different populations and families were divided to compare growth rate and survival of half-sibs in two environments. Growth rate and survival were assessed using capture-recapture techniques. Growth rate was plastic in response to postnatal conditions and did not differ between populations of origin. Survival differed between populations of origin, partially because of differences in neonatal body length. The response of juvenile body length and body condition to selection in the different habitats was affected by the population of origin. This result cannot be simply interpreted in terms of adaptation; however, phenotypic plasticity of fecundity or juvenile size most probably resulted in adaptive reproductive strategies. Adaptation to the habitat by means of genetic specialization was not detected. Further investigation is needed to discriminate between genetic and long-term maternal effects.     

Thermal effects on reptile reproduction: adaptation and phenotypic plasticity in a montane lizard

Interspecific comparisons suggest a strong association between cool climates and viviparity in reptiles. However, intraspecific comparisons, which provide an opportunity to identify causal pathways and to distinguish facultative (phenotypically plastic) effects from canalized (genetically fixed) responses, are lacking. We documented the reproductive traits in an alpine oviparous lizard, and manipulated thermal regimes of gravid females and their eggs to identify proximate causes of life‐history variation. Embryonic development at oviposition was more advanced in eggs laid by females from high‐elevation populations than in eggs produced by females from lower elevations. In the laboratory, experimentally imposed low maternal body temperatures delayed oviposition and resulted in more advanced embryonic development at oviposition. Warm conditions both in utero and in the nest increased hatching success and offspring body size. Our intraspecific comparisons support the hypothesis that viviparity has evolved in cold‐climate squamates because of the direct fitness advantages that warm temperatures provide developing offspring. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 642–655.     

Geographic variation in body size, sexual size dimorphism and fitness components of a seed beetle: local adaptation versus phenotypic plasticity

Variation in body size, growth and life history traits of ectotherms along latitudinal and altitudinal clines is generally assumed to represent adaptation to local environmental conditions, especially adaptation to temperature. However, the degree to which variation along these clines is due to adaptation vs plasticity remains poorly understood. In addition, geographic patterns often differ between females and males – e.g. sexual dimorphism varies along latitudinal clines, but the extent to which these sex differences are due to genetic differences between sexes vs sex differences in plasticity is poorly understood. We use common garden experiments (beetles reared at 24, 30 and 36°C) to quantify the relative contribution of genetically‐based differentiation among populations vs phenotypic plasticity to variation in body size and other traits among six populations of the seed‐feeding beetle Stator limbatus collected from various altitudes in Arizona, USA. We found that temperature induces substantial plasticity in survivorship, body size and female lifetime fecundity, indicating that developmental temperature significantly affects growth and life history traits of S. limbatus. We also detected genetic differences among populations for body size and fecundity, and genetic differences among populations in thermal reaction norms, but the altitude of origin (and hence mean temperature) does not appear to explain these genetic differences. This and other recent studies suggest that temperature is not the major environmental factor that generates geographic variation in traits of this species. In addition, though there was no overall difference in plasticity of body size between males and females (when averaged across populations), we did find that the degree to which dimorphism changed with temperature varied among populations. Consequently, future studies should be extremely cautious when using only a few study populations to examine environmental effects on sexual dimorphism.     

Metapopulation structure favors plasticity over local adaptation

We describe a model for the evolutionary consequences of plasticity in an environmentally heterogeneous metapopulation in which specialists for each of two alternative environments and one plastic type are initially present. The model is similar to that proposed by Moran (1992) but extends her work to two sites. We show that with migration between sites the plastic type is favored over local specialists across a broad range of parameter space. The plastic type may dominate or be fixed even in an environmentally uniform site, and even if the plasticity has imperfect accuracy or bears some cost such that a local specialist has higher fitness in that site, as long as there is some migration between sites with different distributions of environmental states. These results suggest that differences among taxa in dispersal and hence realized migration rates may play a heretofore unrecognized role in their patterns of adaptive population differentiation. Migration relaxes the thresholds for both environmental heterogeneity and accuracy of plastic response above which plasticity is favored. Furthermore, small changes in response accuracy can dramatically and abruptly alter the evolutionary outcome in the metapopulation. A fitness cost to plasticity will substantially reduce the range of conditions in which the plastic type will prevail only if the cost is both large and global rather than environment specific.     

Phenotypic plasticity and local adaptation favor range expansion of a Neotropical palm

One of the most intriguing questions in plant ecology is which evolutionary strategy allows widely distributed species to increase their ecological range and grow in changing environmental conditions. Phenotypic plasticity and local adaptations are major processes governing species range margins, but little is known about their relative contribution for tree species distribution in tropical forest regions. We investigated the relative role of phenotypic plasticity and local adaptation in the ecological distribution of the widespread palm Euterpe edulis in the Brazilian Atlantic Forest. Genetic sampling and experiments were performed in old‐growth remnants of two forest types with higher (Seasonal Semideciduous Forests vs. Submontane Rainforest) and lower biogeographic association and environmental similarities (Submontane Rainforest vs. Restinga Forest). We first assessed the molecular genetic differentiation among populations, focusing on the group of loci potentially under selection in each forest, using single‐nucleotide polymorphism (SNPs) outliers. Further, we looked for potential adaptive divergence among populations in a common garden experiment and in reciprocal transplants for two plant development phases: seedling establishment and sapling growth. Analysis with outlier loci indicated that all individuals from the Semideciduous Forest formed a single group, while another group was formed by overlapping individuals from Submontane Rainforest and Restinga Forest. Molecular differentiation was corroborated by reciprocal transplants, which yielded strong evidence of local adaptations for seedling establishment in the biogeographically divergent Rainforest and Semideciduous Forest, but not for Restinga Forest and Submontane Rainforest. Phenotypic plasticity for palm seedling establishment favors range expansion to biogeographically related or recently colonized forest types, while persistence in the newly colonized ecosystem may be favored by local adaptations if climatic conditions diverge over time, reducing gene flow between populations. SNPs obtained by next‐generation sequencing can help exploring adaptive genetic variation in tropical trees, which impose several challenges to the use of reciprocal transplants.     

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.     

Functional adaptation and phenotypic plasticity at the cellular and whole plant level

The ability to adaptively alter morphological, anatomical, or physiological functional traits to local environmental variations using external environmental cues is especially well expressed by all terrestrial and most aquatic plants. A ubiquitous cue eliciting these plastic phenotypic responses is mechanical perturbation (MP), which can evoke dramatic differences in the size, shape, or mechanical properties of conspecifics. Current thinking posits that MP is part of a very ancient “stress-perception response system” that involves receptors located at the cell membrane/cell wall interface capable of responding to a broad spectrum of stress-inducing factors. This hypothesis is explored here from the perspective of cell wall evolution and the control of cell wall architecture by unicellular and multicellular plants. Among the conclusions that emerge from this exploration is the perspective that the plant cell is phenotypically plastic.     

Maternal effects provide phenotypic adaptation to local environmental conditions

In outcrossing plants, seed dispersal distance is often less than pollen movement. If the scale of environmental heterogeneity within a population is greater than typical seed dispersal distances but less than pollen movement, an individual's environment will be similar to that of its mother but not necessarily its father. Under these conditions, environmental maternal effects may evolve as a source of adaptive plasticity between generations, enhancing offspring fitness in the environment that they are likely to experience. This idea is illustrated using Campanula americana, an herb that grows in understory and light-gap habitats. Estimates of seed dispersal suggest that offspring typically experience the same light environment as their mother. In a field experiment testing the effect of open vs understory maternal light environments, maternal light directly influenced offspring germination rate and season, and indirectly affected germination season by altering maternal flowering time. Results to date indicate that these maternal effects are adaptive; further experimental tests are ongoing. Evaluating maternal environmental effects in an ecological context demonstrates that they may provide phenotypic adaptation to local environmental conditions.     

Rapid differentiation of plasticity in life history and morphology during invasive range expansion and concurrent local adaptation in the horned beetle Onthophagus taurus

Understanding the interplay between genetic differentiation, ancestral plasticity, and the evolution of plasticity during adaptation to environmental variation is critical to predict populations’ responses to environmental change. However, the role of plasticity in rapid adaptation in nature remains poorly understood. We here use the invasion of the horned beetle Onthophagus taurus in the United States during the last half century to study the contribution of ancestral plasticity and post-invasion evolution of plastic responses in rapid population differentiation. We document latitudinal variation in life history and morphology, including genetic compensation in development time and body size, likely adaptive responses to seasonal constraints in the North. However, clinal variation in development time and size was strongly dependent on rearing temperature, suggesting that population differentiation in plasticity played a critical role in successful adaptation on ecological timescales. Clinal variation in wing shape was independent of ancestral plasticity, but correlated with derived plasticity, consistent with evolutionary interdependence. In contrast, clinal variation in tibia shape aligned poorly with thermal plasticity. Overall, this study suggests that post-invasion evolution of plasticity contributed to range expansions and concurrent adaptation to novel climatic conditions.     

Converse Bergmann cline in a Eucalyptus herbivore,Paropsis atomaria Olivier (Coleoptera: Chrysomelidae): phenotypic plasticity or local adaptation?

Aim  To measure latitude-related body size variation in field-collected Paropsis atomaria Olivier (Coleoptera: Chrysomelidae) individuals and to conduct common-garden experiments to determine whether such variation is due to phenotypic plasticity or local adaptation.
Location  Four collection sites from the east coast of Australia were selected for our present field collections: Canberra (latitude 35°19' S), Bangalow (latitude 28°43' S), Beerburrum (latitude 26°58' S) and Lowmead (latitude 24°29' S). Museum specimens collected over the past 100 years and covering the same geographical area as the present field collections came from one state, one national and one private collection.
Methods  Body size (pronotum width) was measured for 118 field-collected beetles and 302 specimens from collections. We then reared larvae from the latitudinal extremes (Canberra and Lowmead) to determine whether the size cline was the result of phenotypic plasticity or evolved differences (= local adaptation) between sites.
Results  Beetles decreased in size with increasing latitude, representing a converse Bergmann cline. A decrease in developmental temperature produced larger adults for both Lowmead (low latitude) and Canberra (high latitude) individuals, and those from Lowmead were larger than those from Canberra when reared under identical conditions.
Main conclusions  The converse Bergmann cline in P. atomaria is likely to be the result of local adaptation to season length.