Shape Of Reaction Norms Research Articles

The genetics of phenotypic plasticity. XVIII. Developmental limits restrict adaptive plasticity.

After environmental change, the trait evolution needed to rescue a population depends on the functional form of the plastic change (reaction norm) of that trait. Nearly all previous models of plasticity evolution for continuous traits have assumed that the functional form is linear, i.e., no limits on the range of plasticity. This paper examines the effect of developmental limits, modeled as a sigmoidal reaction norm, on evolutionary rescue after an abrupt environmental change and the subsequent evolution of plasticity, including genetic assimilation. We examined four different scenarios: (1) developmental limits only, (2) developmental limits plus a cost of plasticity, (3) developmental limits with developmental noise, and (4) developmental limits plus environmental variation. The probability of evolutionary rescue increased with an increase in phenotypic variation allowed by plastic development. With a smaller limit to the range of the plastic phenotype, the evolution of adaptive plasticity was limited, meaning the evolution of non-plastic genes was necessary. The addition of developmental constraints to the model did not speed up genetic assimilation, suggesting new theory is needed to understand empirical observations. The modeling framework presented here could be extended to different ecological and evolutionary conditions, alternative reaction norm shapes, the evolution of additional reaction norm parameters such as the range or the location of the inflection point on the environmental axis, or other function-valued traits.

Pivotal temperature is not for everyone: Evidence for temperature-dependentsex determination in three gecko species.

The prevalence of environmental sex determination (ESD) in squamate reptiles is often overestimated in the literature. This is surprising because we have reliable data demonstrating ESD in only a few species. The documentation of ESD in three species of geckos presented here has significantly increased our knowledge, given that satisfactory evidence for ESD existed in only eight other gecko species. For the first time, we document the occurrence of ESD in the family Sphaerodactylidae. Our finding of unexpected variability in the shapes of reaction norms among geckos highlights that traditional descriptions using parameters such as pivotal temperature, that is, temperature producing a 50:50 sex ratio, are unsatisfactory. For example, the gecko Pachydactylus tigrinus lacks any pivotal temperature and its sex ratios are strongly female-biased across the entire range of viable temperatures. We argue for the effective capture of the relationship between temperature and sex ratio using specific nonlinear models rather than using classical simplistic descriptions and classifications of reaction norms.

Revealing Interactions between Temperature and Salinity and Their Effects on the Growth of Freshwater Diatoms by Empirical Modelling

Salinization and warming are of increasing concern for freshwater ecosystems. Interactive effects of stressors are often studied in bifactorial, two-level experimental setups. The shape of environmental reaction norms and the position of the “control” conditions along them, however, can influence the sign and magnitude of individual responses as well as interactive effects. We empirically model binary-stressor effects in the form of three-dimensional reaction norm surfaces. We monitored the growth of clonal cultures of six freshwater diatoms, Cymbella cf. incurvata, Nitzschia linearis, Cyclotella meneghiniana, Melosira varians, Ulnaria acus, and Navicula gregaria at various temperature (up to 28 °C) and salinity (until the growth ceased) shock treatments. Fitting a broad range of models and comparing them using the Akaike information criterion revealed a large heterogeneity of effects. A bell-shaped curve was often observed in the response of the diatoms to temperature changes, while their growth tended to decrease with increasing electrical conductivity. C. meneghiniana was more tolerant to temperature, whilst C. incurvata and C. meneghiniana were the most sensitive to salinity changes. Empirical modelling revealed interactive effects of temperature and salinity on the slope and the breadth of response curves. Contrasting types of interactions indicates uncertainties in the estimation by empirical modelling.

Evolution of thermal tolerance and phenotypic plasticity under rapid and slow temperature fluctuations.

Global warming is associated with an increase in sea surface temperature and its variability. The consequences of evolving in variable, fluctuating environments are explored by a large body of theory: when populations evolve in fluctuating environments the frequency of fluctuations determines the shapes of tolerance curves (indicative of habitats that organisms can inhabit) and trait reaction norms (the phenotypes that organisms display across these environments). Despite this well-established theoretical backbone, predicting how trait and tolerance curves will evolve in organisms at the foundation of marine ecosystems remains a challenge. Here, we used a globally distributed phytoplankton, Thalassiosira pseudonana, and show that fluctuations in temperature on scales of 3–4 generations rapidly selected for populations with enhanced trait plasticity and elevated thermal tolerance. Fluctuations spanning 30–40 generations selected for the formation of two stable, genetically and physiologically distinct populations, one evolving high trait plasticity and enhanced thermal tolerance, and the other, akin to samples evolved under constant warming, with lower trait plasticity and a smaller increase in thermal tolerance.

Diapause and bet‐hedging strategies in insects: a meta‐analysis of reaction norm shapes

Many organisms escape from lethal climatological conditions by entering a resistant resting stage called diapause, which needs to be optimally timed with seasonal change. As climate change exerts selection pressure on phenology, the evolution of mean diapause timing, but also of phenotypic plasticity and bet‐hedging strategies is expected. The potential of the latter strategy as a means of coping with environmental unpredictability has received little attention in the climate change literature.Populations should be adapted to spatial variation in local conditions; contemporary patterns of phenological strategies across a geographic range may hence provide information about their evolvability. We thus extracted 458 diapause reaction norms from 60 studies. First, we correlated mean diapause timing with mean winter onset. Then we partitioned the reaction norm variance into a temporal component (phenotypic plasticity) and among‐offspring variance (diversified bet‐hedging) and correlated this variance composition with variability of winter onset. Mean diapause timing correlated reasonably well with mean winter onset, except for populations at high latitudes, which apparently failed to track early onsets. Variance among offspring was, however, limited and correlated only weakly with environmental variability, indicating little scope for bet‐hedging. The apparent lack of phenological bet‐hedging strategies may pose a risk in a less predictable climate, but we also highlight the need for more data on alternative strategies.

Phenotypic plasticity under rapid global changes: The intrinsic force for future seagrasses survival.

Coastal oceans are particularly affected by rapid and extreme environmental changes with dramatic consequences for the entire ecosystem. Seagrasses are key ecosystem engineering or foundation species supporting diverse and productive ecosystems along the coastline that are particularly susceptible to fast environmental changes. In this context, the analysis of phenotypic plasticity could reveal important insights into seagrasses persistence, as it represents an individual property that allows species’ phenotypes to accommodate and react to fast environmental changes and stress. Many studies have provided different definitions of plasticity and related processes (acclimation and adaptation) resulting in a variety of associated terminology. Here, we review different ways to define phenotypic plasticity with particular reference to seagrass responses to single and multiple stressors. We relate plasticity to the shape of reaction norms, resulting from genotype by environment interactions, and examine its role in the presence of environmental shifts. The potential role of genetic and epigenetic changes in underlying seagrasses plasticity in face of environmental changes is also discussed. Different approaches aimed to assess local acclimation and adaptation in seagrasses are explored, explaining strengths and weaknesses based on the main results obtained from the most recent literature. We conclude that the implemented experimental approaches, whether performed with controlled or field experiments, provide new insights to explore the basis of plasticity in seagrasses. However, an improvement of molecular analysis and the application of multi‐factorial experiments are required to better explore genetic and epigenetic adjustments to rapid environmental shifts. These considerations revealed the potential for selecting the best phenotypes to promote assisted evolution with fundamental implications on restoration and preservation efforts.

Transgenerational Plasticity and Bet-Hedging: A Framework for Reaction Norm Evolution

Decision-making under uncertain conditions favors bet-hedging (avoidance of fitness variance), whereas predictable environments favor phenotypic plasticity. However, entirely predictable or entirely unpredictable conditions are rarely found in nature. Intermediate strategies are required when the time lag between information sensing and phenotype induction is large (e.g., transgenerational plasticity) and when cues are only partially predictive of future conditions. Nevertheless, current theory regards plasticity and bet-hedging as distinct entities. We here develop a unifying framework: based on traits with binary outcomes like seed germination or diapause incidence we clarify that diversified bet-hedging (risk-spreading among one’s offspring) and transgenerational plasticity are mutually exclusive strategies, arising from opposing changes in reaction norms (allocating phenotypic variance among or within environments). We further explain the relationship of this continuum with arithmetic mean maximization vs. conservative bet-hedging (a risk-avoidance strategy), and canalization vs. phenotypic variance in a three-dimensional continuum of reaction norm evolution. We discuss under which scenarios costs and limits may constrain the evolution of reaction norm shapes.

Climate‐related geographical variation in performance traits across the invasion front of a widespread non‐native insect

AbstractAimInvasive species are ideal systems for testing geographical differences in performance traits and measuring evolutionary responses as a species spreads across divergent climates and habitats. The European gypsy moth, Lymantria dispar dispar L. (Lepidoptera: Erebidae), is a generalist forest defoliator introduced to Medford, Massachusetts, USA in 1869. The invasion front extends from Minnesota to North Carolina and the ability of this species to adapt to local climate may contribute to its continuing spread. We evaluated the performance of populations along the climatic gradient of the invasion front to test for a relationship between climate and ecologically important performance traits.LocationEastern United States of AmericaTaxonLymantria dispar dispar L. (Lepidoptera: Erebidae)MethodsInsects from 14 populations across the US invasion front and interior of the invasive range were reared from hatch to adult emergence in six constant temperature treatments. The responses of survival, pupal mass and larval development time were analysed as a function of source climate (annual mean normal temperature), rearing temperature and their interaction using multiple polynomial regression.ResultsWith the exception of female development time, there were no significant interactions between source climate and rearing temperature, indicating little divergence in the shape of thermal reaction norms among populations. Source population and rearing temperature were significant predictors of survival and pupal mass. Independent of rearing temperature, populations from warmer climates had lower survival than those from colder climates, but attained larger body size despite similar development times. Larval development time was dependent on rearing temperature, but there were not consistent relationships with source climate.Main ConclusionsThermal adaptation can be an important factor shaping the spread of invasive species, particularly in the context of climate change. Our results suggest that L. d. dispar is highly plastic, but has undergone climate‐related adaptation in thermal performance and life‐history traits as it spread across North America.

When to diapause or not to diapause? Winter predictability is not the answer

A recommendation of: Jens Joschinski and Dries Bonte Diapause is not selected as a bet-hedging strategy in insects: a meta-analysis of reaction norm shapes 10.1101/752881

Reaction norms for heat tolerance and evaporative cooling capacity do not vary across a climatic gradient in a passerine bird

There is increasing evidence for considerable phenotypic flexibility in endotherm thermal physiology, a phenomenon with far-reaching implications for the evolution of traits related to heat tolerance. Numerous studies have documented intraspecific variation in avian thermoregulatory traits, but few have revealed the shapes of thermoregulatory reaction norms or how these might vary among populations. We investigated phenotypic flexibility in the ability of a model Afrotropical passerine bird (the white-browed sparrow-weaver, Plocepasser mahali) to handle high air temperatures (Ta). We allocated birds from three sites varying by ~ 11 °C in mean daily summer maximum Ta to three acclimation temperature (Taccl) treatments (daytime Taccl ≈ 30 °C, 36 °C or 42 °C respectively; n ≈ 10 per site per Taccl). After an acclimation period of 30 days, heat tolerance and evaporative cooling capacity was quantified by exposing birds to progressively higher Ta until they approached severe hyperthermia (body temperature [Tb] = 44.5 °C; Ta range: 38–54 °C). We measured metabolic rate and evaporative water loss using open flow-through respirometry, and Tb using temperature-sensitive passive-integrated transponder tags. Hyperthermia threshold Ta (Ta,HT) was significantly higher and Tb significantly lower in birds acclimated to the hottest Taccl compared to those from milder acclimation treatments. Population (i.e., site of capture) was not a significant predictor of any thermoregulatory variables or hyperthermia threshold Ta (Ta,HT) after acclimation, revealing that the shape of reaction norms for heat tolerance and evaporative cooling capacity does not vary among these three populations.

Phytoplankton adaptation in ecosystem models

We compare two different approaches to model adaptation of phytoplankton through trait value changes. Both consider mutation and selection (MuSe) but differ with respect to the underlying conceptual framework. The first one (MuSe-IBM) explicitly considers a population of individuals that are subject to random mutation during cell division. The second is a deterministic multi-compartment model (MuSe-MCM) that considers numerous genotypes of the population and where mutations are treated as a transfer of biomass between neighboring genotypes (i.e., a diffusion of characteristics in trait space). Focusing on the adaptation of optimal temperature, we show model results for different scenarios: a sudden change in environmental temperature, a seasonal variation and high frequency fluctuations. In addition, we investigate the effect of different shapes of thermal reaction norms as well as the role of alternating growth and resting phases on the adaptation process. For all cases, the differences between MuSe-IBM and MuSe-MCM are found to be negligible. Both models produce a number of well-known and plausible features. While the IBM has the advantage of including more mechanistic (i.e., probabilistic) processes, the MCM is much less computationally demanding and therefore suitable for implementation in three-dimensional ecosystem models.

Impacts of increased ocean temperatures on a low-latitude coral reef fish – Processes related to oxygen uptake and delivery

Increasing temperatures are expected to significantly affect the physiological performance of ectotherms, particularly in tropical locations. The shape of an organism's thermal reaction norm can provide important information on its capacity to persist under climate change scenarios; however, difficulty lies in choosing a measurable trait that best depicts physiological performance. This study investigated the effects of elevated temperatures on processes related to oxygen uptake and delivery, including oxygen consumption, haematology, and tissue health for a low-latitude population of coral reef damselfish. Acanthochromis polyacanthus were collected from the Torres Strait (10°31–46′S, 142°20–35′E) and maintained at current average ocean temperatures (+0 °C; seasonally cycling), + 1.5 °C and + 3 °C higher than present day temperatures for 10 months. Aerobic performance indicated a limit to metabolic function at + 3 °C (33 °C), following an increase in aerobic capacity at + 1.5 °C (31.5 °C). Neither haematological parameters nor gill morphology showed the same improvement in performance at + 1.5 °C. Gill histopathology provided the first indicator of a decline in organism health, which corresponded with mortality observations from previous research. Findings from this study suggest thermal specialisation in this low-latitude population as well as variation in thermal sensitivity, depending on the physiological trait.

Developmental temperatures and phenotypic plasticity in reptiles: a systematic review and meta-analysis.

Early environments can profoundly influence an organism in ways that persist over its life. In reptiles, early thermal environments (nest temperatures) can impact offspring phenotype and survival in important ways, yet we still lack an understanding of whether general trends exist and the magnitude of impact. Understanding these patterns is important in predicting how climate change will affect reptile populations and the role of phenotypic plasticity in buffering populations. We compiled data from 175 reptile studies to examine, and quantify, the effect of incubation temperature on phenotype and survival. Using meta-analytic approaches (standardized mean difference between incubation treatments, Hedges' g), we show that across all trait types examined there is, on average, a moderate to large magnitude of effect of incubation temperatures (absolute effect: |g| = 0.75). Unsurprisingly, this influence was extremely large for incubation duration, as predicted, with warmer temperatures decreasing incubation time overall (g = -8.42). Other trait types, including behaviour, physiology, morphology, performance, and survival experienced reduced, but still mostly moderate to large effects, with particularly strong effects on survival. Moreover, the impact of incubation temperature persisted at least one-year post-hatching, suggesting that these effects have the potential to impact fitness in the long term. The magnitude of effect increased as the change in temperature increased (e.g. 6°C versus 2°C) in almost all cases, and tended to decrease when temperatures of the treatments fluctuated around a mean temperature compared to when they were constant. The effect also depended on the mid-temperature of the comparison, but not in consistent ways, with some traits experiencing the greatest effects at extreme temperatures, while others did not. The highly heterogeneous nature of the effects we observe, along with a large amount of unexplained variability, indicates that the shape of reaction norms between phenotype and temperature, along with ecological and/or experimental factors, are important when considering general patterns. Our analyses provide new insights into the effects of incubation environments on reptile phenotype and survival and allow general, albeit coarse, predictions for taxa experiencing warming nest temperatures under climatic change.

Advancing meta-analysis beyond simple parameter estimation.

Advancing meta-analysis beyond simple parameter estimation.

Evolutionary divergence of reaction norms in ecological context: a commentary.

Evolutionary divergence of reaction norms in ecological context: a commentary.

Variation in reaction norms: Statistical considerations and biological interpretation

Analysis of reaction norms, the functions by which the phenotype produced by a given genotype depends on the environment, is critical to studying many aspects of phenotypic evolution. Different techniques are available for quantifying different aspects of reaction norm variation. We examine what biological inferences can be drawn from some of the more readily applicable analyses for studying reaction norms. We adopt a strongly biologically motivated view, but draw on statistical theory to highlight strengths and drawbacks of different techniques. In particular, consideration of some formal statistical theory leads to revision of some recently, and forcefully, advocated opinions on reaction norm analysis. We clarify what simple analysis of the slope between mean phenotype in two environments can tell us about reaction norms, explore the conditions under which polynomial regression can provide robust inferences about reaction norm shape, and explore how different existing approaches may be used to draw inferences about variation in reaction norm shape. We show how mixed model-based approaches can provide more robust inferences than more commonly used multistep statistical approaches, and derive new metrics of the relative importance of variation in reaction norm intercepts, slopes, and curvatures.

Fish life history dynamics: shifts in prey size structure evoke shifts in predator maturation traits

A bioenergetic framework is developed to predict optimal life history responses to environmentally driven changes in the rate of energy production by a predator. This framework is used to predict the responses of age at maturation, size at maturation, and asymptotic size to changes in the predator–prey size ratio. Predators feeding on relatively smaller prey (i.e., having larger predator–prey size ratios) have lower growth efficiency and are predicted as a consequence to mature earlier, at smaller sizes, and reach smaller asymptotic sizes. This prediction was tested using a 78-year time series (1936–2013) of data from a natural population of lake trout (Salvelinus namaycush) in Lake Opeongo, Algonquin Park, Ontario, Canada. A large decrease in the predator–prey size ratio for this population occurred over the period 1950–1965 when a preferred prey (cisco, Coregonus artedii) was introduced to the lake. This decrease was followed by ∼20 years of constancy in the size ratio and then 25 years of progressive increase. Lake trout life history responded plastically during both periods and consistently with our predictions. Extensive analysis of available data provided little empirical support for alternative explanations for the observed changes in lake trout size and maturity (e.g., changes in cisco and (or) lake trout density and harvest rates). The framework developed here derives plastic life history changes from fixed developmental thresholds that are based on the scaling of net production with body size and can be used to predict the shape of maturation reaction norms for the major shifts in community structure that are compactly summarized by changes in size spectrum parameters.

Keeping your options open: Maintenance of thermal plasticity during adaptation to a stable environment.

Phenotypic plasticity may allow species to cope with environmental variation. The study of thermal plasticity and its evolution helps understanding how populations respond to variation in temperature. In the context of climate change, it is essential to realize the impact of historical differences in the ability of populations to exhibit a plastic response to thermal variation and how it evolves during colonization of new environments. We have analyzed the real-time evolution of thermal reaction norms of adult and juvenile traits in Drosophila subobscura populations from three locations of Europe in the laboratory. These populations were kept at a constant temperature of 18ºC, and were periodically assayed at three experimental temperatures (13ºC, 18ºC, and 23ºC). We found initial differentiation between populations in thermal plasticity as well as evolutionary convergence in the shape of reaction norms for some adult traits, but not for any of the juvenile traits. Contrary to theoretical expectations, an overall better performance of high latitude populations across temperatures in early generations was observed. Our study shows that the evolution of thermal plasticity is trait specific, and that a new stable environment did not limit the ability of populations to cope with environmental challenges.

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

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

Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria

Rising temperatures are expected to favour the growth of bloom-forming cyanobacteria in temperate lakes, but may also change the composition of cyanobacterial communities. To predict future community and bloom dynamics, it is therefore important to understand how bloom-forming species respond to temperature. Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju is an invasive, toxin-producing, nitrogen-fixer that may benefit from warming. To understand how changing temperatures will influence its ability to compete against native North American bloom-formers, we characterized the thermal reaction norms and temperature traits of three C. raciborskii strains, four strains of Microcystis aeruginosa (Kutzing) Kutzing and one strain of Anabaena flos-aquae (Lyng.) Breb. C. raciborskii strains had higher optimum temperatures and survived higher temperatures than toxic M. aeruginosa strains, but had no apparent advantage over the non-toxic M. aeruginosa strain or A. flos-aquae. M. aeruginosa strains and A. flos-aquae tolerated lower temperatures than C. raciborskii, suggesting that fitness differences at low temperature may be important in limiting the latter’s spread. Furthermore, we found that nutrient availability strongly influenced thermal reaction norm shape: nitrogen deprivation lowered growth rates and decreased both low- and high-temperature tolerance, but did not affect the optimum temperature in C. raciborskii.