Plasticity in probabilistic reaction norms for maturation in a salmonid fish

The relationship between body size and the probability of maturing, often referred to as the probabilistic maturation reaction norm (PMRN), has been increasingly used to infer genetic variation in maturation schedule. Despite this trend, few studies have directly evaluated plasticity in the PMRN. A transplant experiment using white-spotted charr demonstrated that the PMRN for precocious males exhibited plasticity. A smaller threshold size at maturity occurred in charr inhabiting narrow streams where more refuges are probably available for small charr, which in turn might enhance the reproductive success of sneaker precocious males. Our findings suggested that plastic effects should clearly be included in investigations of variation in PMRNs.     

Measuring probabilistic reaction norms for age and size at maturation

We present a new probabilistic concept of reaction norms for age and size at maturation that is applicable when observations are carried out at discrete time intervals. This approach can also be used to estimate reaction norms for age and size at metamorphosis or at other ontogenetic transitions. Such estimations are critical for understanding phenotypic plasticity and life-history changes in variable environments, assessing genetic changes in the presence of phenotypic plasticity, and calibrating size- and age-structured population models. We show that previous approaches to this problem, based on regressing size against age at maturation, give results that are systematically biased when compared to the probabilistic reaction norms. The bias can be substantial and is likely to lead to qualitatively incorrect conclusions; it is caused by failing to account for the probabilistic nature of the maturation process. We explain why, instead, robust estimations of maturation reaction norms should be based on logistic regression or on other statistical models that treat the probability of maturing as a dependent variable. We demonstrate the utility of our approach with two examples. First, the analysis of data generated for a known reaction norm highlights some crucial limitations of previous approaches. Second, application to the northeast arctic cod (Gadus morhua) illustrates how our approach can be used to shed new light on existing real-world data.     

Population size and identity influence the reaction norm of the rare,endemic plant Cochlearia bavarica across a gradient of environmental stress

Habitat degradation and loss can result in population decline and genetic erosion, limiting the ability of organisms to cope with environmental change, whether this is through evolutionary genetic response (requiring genetic variation) or through phenotypic plasticity (i.e., the ability of a given genotype to express a variable phenotype across environments). Here we address the question whether plants from small populations are less plastic or more susceptible to environmental stress than plants from large populations. We collected seed families from small (<100) versus large natural populations (>1,000 flowering plants) of the rare, endemic plant Cochlearia bavarica (Brassicaceae). We exposed the seedlings to a range of environments, created by manipulating water supply and light intensity in a 2 x 2 factorial design in the greenhouse. We monitored plant growth and survival for 300 days. Significant effects of offspring environment on offspring characters demonstrated that there is phenotypic plasticity in the responses to environmental stress in this species. Significant effects of population size group, but mainly of population identity within the population size groups, and of maternal plant identity within populations indicated variation due to genetic (plus potentially maternal) variation for offspring traits. The environment x maternal plant identity interaction was rarely significant, providing little evidence for genetically- (plus potentially maternally-) based variation in plasticity within populations. However, significant environment x population-size-group and environment x population-identity interactions suggested that populations differed in the amount of plasticity, the mean amount being smaller in small populations than in large populations. Whereas on day 210 the differences between small and large populations were largest in the environment in which plants grew biggest (i.e., under benign conditions), on day 270 the difference was largest in stressful environments. These results show that population size and population identity can affect growth and survival differently across environmental stress gradients. Moreover, these effects can themselves be modified by time-dependent variation in the interaction between plants and their environment.     

Determination of body shape variation in Irish hatchery‐reared and wild Atlantic salmon

Discriminant function analysis was used to distinguish morphologically between samples of parr, smolts and adult Atlantic salmon Salmo salar from several hatchery and river systems in Ireland. The effect of habitat shift was investigated in Atlantic salmon parr. Parr grown from the eyed‐egg stage with a non‐sibling group in a hatchery environment, came to resemble the mean body shape of their host hatchery Atlantic salmon stock more closely than that of a full sibling group grown at their natal hatchery. Wild Atlantic salmon smolts differed in shape from hatchery‐reared smolts. This difference was less pronounced, but still statistically significant when wild adults were compared with hatchery‐reared adults captured in the coastal drift‐net fishery after a year spent at sea. Rearing conditions had a significant impact on the production and growth of fish body shape. This in turn may have affected adaptability and survivorship of ranched Atlantic salmon in the marine environment.     

Contrasting trends in two condition indices: bathymetric and spatial variation in autumn condition of Icelandic cod Gadus morhua

Bathymetric and regional variation in condition of Icelandic cod Gadus morhua in autumn is compared to that previously observed in spring. Once again, contradicting patterns in the hepato-somatic index and a morphometric index of fish condition were observed. The relevance of this persistent spatial variation in condition in relation to emerging evidence of behavioural types is discussed.     

Rule of age and size at maturity: individual variation in the maturation history of resident white-spotted charr

Individual growth and maturation histories, age, and size at maturity of resident white-spotted charr Salvelinus leucomaenis were examined in a tag-recapture study in a natural river over 3 years. Slow-growing fish reached sexual maturity not only at an older age, but also at a smaller size than fast-growing fish, although females had a larger threshold size at maturity than males at each age. It is suggested that these patterns result from adaptive phenotypic plasticity that depends on individual growth conditions.     

The importance of social dimension and maturation stage for the probabilistic maturation reaction norm in Poecilia reticulata

Maturation is an important event in an organism's life history, with important implications on dynamics of both wild and captive populations. The probabilistic maturation reaction norm (PMRN) has emerged as an important method to describe variation in maturation in wild fish. Because most PMRNs are based on age and size only, it is important to understand limitations of these variables in explaining maturation. We experimentally assessed (i) the sensitivity of age‐ and size‐based PMRNs to unaccounted sources of plasticity, (ii) the role of social environment on maturation and (iii) the significance of estimating PMRNs early and late in the maturation process (initiation and completion of maturation, respectively). We reared male guppies (Poecilia reticulata) under laboratory conditions, subjected to two food levels and three different social cues. We found that growth and social environment affected the maturation in a way that could not be accounted for by their effect on age and size. PMRNs estimated for the initiation stage were less plastic (growth differences and social cues influenced the PMRN shape only little) than those for completion. The initiation of maturation is probably closer to the maturation ‘decision’ and allows determining factors influencing maturation decision most accurately.     

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.     

Old wine in new bottles: reaction norms in salmonid fishes

Genetic variability in reaction norms reflects differences in the ability of individuals, populations and ultimately species to respond to environmental change. By increasing our understanding of how genotype × environment interactions influence evolution, studies of genetic variation in phenotypic plasticity serve to refine our capacity to predict how populations will respond to natural and anthropogenic environmental variability, including climate change. Given the extraordinary variability in morphology, behaviour and life history in salmonids, one might anticipate the research milieu on reaction norms in these fishes to be empirically rich and intellectually engaging. Here, I undertake a review of genetic variability in continuous and discontinuous (threshold) norms of reaction in salmonid fishes, as determined primarily (but not exclusively) by common-garden experiments. Although in its infancy from a numerical publication perspective, there is taxonomically broad evidence of genetic differentiation in continuous, threshold and bivariate reaction norms among individuals, families and populations (including inter-population hybrids and backcrosses) for traits as divergent as embryonic development, age and size at maturity, and gene expression. There is compelling inferential evidence that plasticity is heritable and that population differences in reaction norms can reflect adaptive responses, by natural selection, to local environments. As a stimulus for future work, a series of 20 research questions are identified that focus on reaction-norm variability, selection, costs and constraints, demographic and conservation consequences, and genetic markers and correlates of phenotypic plasticity.     

The interaction between predation risk and food ration on behavior and morphology of Eurasian perch

The risk of both predation and food level has been shown to affect phenotypic development of organisms. However, these two factors also influence animal behavior that in turn may influence phenotypic development. Hence, it might be difficult to disentangle the behavioral effect from the predator or resource‐level effects. This is because the presence of predators and high resource levels usually results in a lower activity, which in turn affects energy expenditure that is used for development and growth. It is therefore necessary to study how behavior interacts with changes in body shape with regard to resource density and predators. Here, we use the classic predator‐induced morphological defense in fish to study the interaction between predator cues, resource availability, and behavioral activity with the aim to determine their relative contribution to changes in body shape. We show that all three variables, the presence of a predator, food level, and activity, both additively and interactively, affected the body shape of perch. In general, the presence of predators, lower swimming activity, and higher food levels induced a deep body shape, with predation and behavior having similar effect and food treatment the smallest effect. The shape changes seemed to be mediated by changes in growth rate as body condition showed a similar effect as shape with regard to food‐level and predator treatments. Our results suggests that shape changes in animals to one environmental factor, for example, predation risk, can be context dependent, and depend on food levels or behavioral responses. Theoretical and empirical studies should further explore how this context dependence affects fitness components such as resource gain and mortality and their implications for population dynamics.     

Reaction norm variants for male calling song in populations of Achroia grisella (Lepidoptera: Pyralidae): toward a resolution of the lek paradox

Significant additive genetic variance often occurs for male advertisement traits in spite of the directional selection imposed by female choice, a problem generally known in evolutionary biology as the lek paradox. One hypothesis, which has limited support from recent studies, for the resolution of this paradox is the role of genotype x environment interaction in which no one genotype exhibits the superior performance in all environments--a crossover of reaction norms. However, these studies have not characterized the actual variation of reaction norms present in natural populations, and the extent to which crossover maintains genetic variance remains unknown. Here, we present a study of genotype x environment interaction for the male calling song in populations of Achroia grisella (Lepidoptera: Pyralidae; lesser waxmoth). We report significant variance among reaction norms for male calling song in two North American populations of A. grisella as measured along temperature, food availability, and density gradients, and there is a relatively high incidence of crossover of the temperature reaction norms. This range of reaction norm variants and their crossover may reflect the co-occurrence of plastic and canalized genotypes, and we argue that the different responses of these variants along environmental gradients may contribute toward the maintenance of genetic variance for male song.     

Epigenetic regulation of trophic morphology through feeding behaviour in Arctic charr, Salvelinus alpinus

Several models of speciation suggest that in species that are phenotypically plastic, selection can act on phenotypic variation that is environmentally induced in the earliest stages of divergence. One trait that could be subject to this process is foraging behaviour, where discrete foraging strategies are common. One species which is highly plastic in the expression of phenotype, the Arctic charr, Salvelinus alpinus (L.), is characterized by discrete variation in the anatomy of the head and mouthparts. These traits have been shown to have a functional significance, but the expression of which is thought to be at least partly phenotypically plastic. Here we test the hypothesis that foraging behaviour may regulate the anatomy of the head and mouthparts in Arctic charr. In a dyad experiment, size‐matched pairs of fish from a mixed family group were fed a diet of either Mysis (a hard‐bodied shrimp) or Chironomid larvae. Nine morphometric measures of head dimensions that describe wild trophic morphs were measured at the start of the experiment and 24 weeks later. Principal component scores of size‐corrected morphometric measures showed highly significant differences between fish exposed to the two diets. Univariate ANOVA analysis of the head morphometric variables showed that fish fed on Chironomids developed longer, wider jaws, longer heads and a larger eye for a given body length than did those fish fed upon Mysis. We conclude that foraging anatomy in Arctic charr is phenotypically plastic and that variation in foraging behaviour that results in feeding specialization in the wild could induce variation in head anatomy. This in turn could reinforce foraging specialization. Very rapid epigenetic divergence into distinct feeding morphs (as demonstrated here) would allow selection to act at more than one mode and thus could promote rapid evolutionary divergence, initially prior to genetic segregation, in species which are highly plastic. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78 , 43–49.     

Probabilistic maturation reaction norms assessed from mark–recaptures of wild fish in their natural habitat

Reaction norms are a valuable tool in evolutionary biology. Lately, the probabilistic maturation reaction norm approach, describing probabilities of maturing at combinations of age and body size, has been much applied for testing whether phenotypic changes in exploited populations of fish are mainly plastic or involving an evolutionary component. However, due to typical field data limitations, with imperfect knowledge about individual life histories, this demographic method still needs to be assessed. Using 13 years of direct mark–recapture observations on individual growth and maturation in an intensively sampled population of brown trout (Salmo trutta), we show that the probabilistic maturation reaction norm approach may perform well even if the assumption of equal survival of juvenile and maturing fish does not hold. Earlier studies have pointed out that growth effects may confound the interpretation of shifts in maturation reaction norms, because this method in its basic form deals with body size rather than growth. In our case, however, we found that juvenile body size, rather than annual growth, was more strongly associated with maturation. Viewed against earlier studies, our results also underscore the challenges of generalizing life‐history patterns among species and populations.     

The reaction norm for abdominal pigmentation and its curve in Drosophila mediopunctata depend on the mean phenotypic value

The idea of a general independence between the phenotypic plasticity and the mean value of a trait is, presently, a consensus. Here, we use the reaction norm of abdominal pigmentation (number of dark spots) of Drosophila mediopunctata in response to temperature, to test this idea. We raised eight strains, bearing two different chromosomal inversions and with varying mean phenotypic values, under 11 temperatures in a thermal gradient to test for predictions concerning mean phenotypic values, chromosomal inversions, and reaction norms. Our results revealed a strong effect of different phenotypic groups and no effect of different karyotypes on reaction norms. Moreover, we found a significant negative correlation between mean phenotypic value and the curvature of the reaction norms, revealing a high dependency of the reaction norm shape on mean phenotypic value. These results clearly reject the idea of genetic independence between mean value and phenotypic plasticity, and may indicate a pattern of correlation, which may include results from other traits and species, with an importance that has not been fully appreciated.     

The evolution of reaction norms: simple models for age and size at maturity

This paper presents a simple model for the evolution of reaction norms for age and size at maturity that predicts reaction norms with a variety of shapes. Using realistic parameter values the model predicts reaction norms close to those observed in Drosophila. The major assumptions of the model are: 1) that net reproductive rate is maximized, 2) that growth is determinate, and 3) that mortality rates are independent of age and size at maturity. If, additionally, juvenile mortality is uncorrelated with a growth coefficient, k, the model predicts that selection favors maturation later at a smaller size when k is reduced by environmental factors and that decreased juvenile mortality leads to delayed maturity. These two predictions conform with those found by previous models using other measures of fitness. Correlations between k and juvenile mortality can change the shape of the predicted reaction norm. Depending on the precise form of the correlation, the model can predict done- or bowl-shaped reaction norms and can predict delayed or earlier maturity as k decreases. These shapes are qualitatively different from those predicted by previous models that used different fitness measures. Systematic estimates of the parameter values for this and for related models are required to determine the appropriate fitness measure for models of reaction norms.     

Phenotypic Correlation of Juvenile Growth Rate between Different Consecutive foraging Environments in a Salmonid fish: A Field Experiment

Many organisms occupy considerably different environments during individual's lifespan. We are interested in how the phenotypic characteristics that are favourable in the earlier environment predict fitness in the later environment. High predictability of fitness between the two consecutive environments suggests that the either the same traits are favored in both environments, or that the favourable traits are genetically correlated. In this study, we ask how similarity of consecutive foraging environments affects the phenotypic correlation of juvenile brown trout growth rate. More specifically, we used a genetically narrow stock of hatchery-bred fish to contrast individual growth rates between high and low density hatchery environments, and thereafter between hatchery and natural lake environment. As expected, growth rate was highly dependent on the environment, and the fish showed considerable phenotypic plasticity. Furthermore, we found a strong positive correlation in growth rate between similar foraging environments, for example, between high and low density hatchery stocks, and between hatchery and a lake with small fish as main prey. However, hatchery growth did not predict growth rate in lakes where fish had to forage on bottom-dwelling invertebrates. Our results suggest that when the consecutive environments differed dramatically with respect to traits that fish use for foraging, relative performance of individual fish changed, earlier performance not being an accurate predictor of performance in the new environment. In this case, fitness of the fish was determined by an environment-specific set of traits that were not the same between the two consecutive environments. The result indicates that assessment of individual performance may be highly environment specific in trout. This revised version was published online in July 2006 with corrections to the Cover Date.     

Sex-specific plasticity of growth and maturation size in a spider: implications for sexual size dimorphism

Sex-specific plasticity in body size has been recently proposed to cause intraspecific patterns of variation in sexual size dimorphism (SSD). We reared juvenile male and female Mediterranean tarantulas (Lycosa tarantula) under two feeding regimes and monitored their growth until maturation. Selection gradients calculated across studies show how maturation size is under net stabilizing selection in females and under directional selection in males. This pattern was used to predict that body size should be more canalized in females than in males. As expected, feeding affected male but not female maturation size. The sex-specific response of maturation size was related to a dramatic divergence between subadult male and female growth pathways. These results demonstrate the existence of sex-specific canalization and resource allocation to maturation size in this species, which causes variation in SSD depending on developmental conditions consistent with the differential-plasticity hypothesis explaining Rensch's Rule.     

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.