DOES SIZE MATTER MOST? THE EFFECT OF GROWTH HISTORY ON PROBABILISTIC REACTION NORM FOR SALMON MATURATION

Body size is widely believed to affect the occurrence of sexual maturation. Recent studies have used changes in the age-specific body size at which the probability of maturing is 50%, a feature of probabilistic reaction norms, to quantify purported evolution of life histories. However, body size results from a combination of growth rates during successive developmental stages. Therefore, to understand the evolution of the maturation schedule, it is necessary to comprehend the relationships among body size, growth history, and maturation schedule. We examined the relationships among body size, previous growth history, and maturation probability in chum salmon (Oncorhynchus keta). In this study, previous growth history was estimated from yearly specific growth increments that provide information describing body size. Previous growth history was found to be more closely linked to maturation probability than body size. The most recent growth condition was the most important factor affecting whether a fish matured during the subsequent breeding season. Because individuals of similar body size and same age can have different growth histories, the relationship between body size and maturation probability could be plastically modified by growth history. This may violate an assumption required to infer evolution, namely that size-related maturation trends in probabilistic reaction norms are immune to growth history.     

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.     

THE EVOLUTION OF PHENOTYPIC PLASTICITY IN LIFE-HISTORY TRAITS: PREDICTIONS OF REACTION NORMS FOR AGE AND SIZE AT MATURITY

We used life-history theory to predict reaction norms for age and size at maturation. We assumed that fecundity increases with size and that juvenile mortality rates of offspring decrease as ages-at-maturity of parents increase, then calculated the reaction norm by varying growth rate and calculating an optimal age at maturity for each growth rate. The reaction norm for maturation should take one of at least four shapes that depend on specific relations between changes in growth rates and changes in adult mortality rates, juvenile mortality rates, or both. Most organisms should mature neither at a fixed size nor at a fixed age, but along an age-size trajectory. The model makes possible a clear distinction between the genetic and phenotypic components of variation. The evolved response to selection is reflected in the shape and position of the reaction norm. The phenotypic response of a single organism to rapid or slow growth is defined by the location of its maturation event as a point on the reaction norm. A quantitative test with data from 19 populations and species of fish showed that predictions were in good agreement with observations (r = 0.93, P < 0.0001). The predictions of the model also agreed qualitatively with observed phenotypic variation in age and size at maturity in humans, platyfish, fruit flies, and red deer. This preliminary success suggests that experiments designed to test the predictions directly will be worthwhile.     

Ecological and evolutionary patterns of freshwater maturation in Pacific and Atlantic salmonines

Reproductive tactics and migratory strategies in Pacific and Atlantic salmonines are inextricably linked through the effects of migration (or lack thereof) on age and size at maturity. In this review, we focus on the ecological and evolutionary patterns of freshwater maturation in salmonines, a key process resulting in the diversification of their life histories. We demonstrate that the energetics of maturation and reproduction provides a unifying theme for understanding both the proximate and ultimate causes of variation in reproductive schedules among species, populations, and the sexes. We use probabilistic maturation reaction norms to illustrate how variation in individual condition, in terms of body size, growth rate, and lipid storage, influences the timing of maturation. This useful framework integrates both genetic and environmental contributions to conditional strategies for maturation and, in doing so, demonstrates how flexible life histories can be both heritable and subject to strong environmental influences. We review evidence that the propensity for freshwater maturation in partially anadromous species is predictable across environmental gradients at geographic and local spatial scales. We note that growth is commonly associated with the propensity for freshwater maturation, but that life-history responses to changes in growth caused by temperature may be strikingly different than changes caused by differences in food availability. We conclude by exploring how contemporary management actions can constrain or promote the diversity of maturation phenotypes in Pacific and Atlantic salmonines and caution against underestimating the role of freshwater maturing forms in maintaining the resiliency of these iconic species.     

An empirical test for a zone of canalization in thermal reaction norms

Theoretical models on the evolution of phenotypic plasticity predict a zone of canalization where reaction norms cross, and genetic variation is minimized in the environment a population most frequently encounter. Empirical tests of this prediction are largely missing, in particular for life‐history traits. We addressed this prediction by quantifying thermal reaction norms of three life‐history traits (somatic growth rate, age and size at maturation) of a Norwegian population of Daphnia magna and testing for the occurrence of an intermediate temperature (T_m) at which genetic variance in the traits is minimized. Size at maturation changed relatively little with temperature compared to the other traits, and there was no genetic variance in the shape of the reaction norm. Consequently, age at maturation and somatic growth rate were strongly negatively correlated. Both traits showed a strong genotype–environment interaction, and the estimated T_m was 14 °C for both age at maturation and growth rate. This value of T_m corresponds well with mean summer temperatures experienced by the population and suggests that the population has evolved under stabilizing selection in temperatures that fluctuate around this mean temperature. These results suggest local adaptation to temperature in the studied population and allow predicting evolutionary trajectories of thermal reaction norms under changing thermal regimes.     

Host plant adaptation and the evolution of thermal reaction norms

For most ectotherms, increasing the rearing temperature reduces the final (adult) body size, producing a negative slope for the thermal reaction norm. Recent studies show that this relationship may be reversed under conditions of low resource quality, producing a positive slope for the thermal reaction norm. If populations or species differ in the degree of evolutionary adaptation to a resource, how does this differential adaptation alter their thermal reaction norms? We used a common garden experiment with the tobacco hornworm, Manduca sexta, to address this question. We examined the thermal reaction norms for body size of two populations of M. sexta that differ in their evolutionary exposures to an atypical, low-quality resource (devil's claw; Proboscidea louisianica), but have comparable exposures to a typical, high-quality resource (tobacco; Nicotiana tabacum). Both populations had increased mean larval mortalities and development times when reared on devil's claw compared with tobacco, but the magnitudes of these increases differed between populations. Both populations had similar, negatively sloped thermal reaction norms on the typical, high-quality resource (tobacco), but had divergent, non-negative thermal reaction norms on the atypical, low-quality resource (devil's claw): the population with the longer evolutionary history of exposure to the atypical resource exhibited a flat (rather than positive) reaction norm. These results suggest that population differences in host plant adaptation can predictably influence the slopes of thermal reaction norms.     

A multi-population approach supports common patterns in marine growth and maturation decision in Atlantic salmon (Salmo salar L.) from southern Europe

This study provides a regional picture of long-term changes in Atlantic salmon growth at the southern edge of their distribution, using a multi-population approach spanning 49 years and five populations. We provide empirical evidence of salmon life history being influenced by a combination of common signals in the marine environment and population-specific signals. We identified an abrupt decline in growth from 1976 and a more recent decline after 2005. As these declines have also been recorded in northern European populations, our study significantly expands a pattern of declining marine growth to include southern European populations, thereby revealing a large-scale synchrony in marine growth patterns for almost five decades. Growth increments during their sea sojourn were characterized by distinct temporal dynamics. At a coarse temporal resolution, growth during the first winter at sea seemed to gradually improve over the study period. However, the analysis of finer seasonal growth patterns revealed ecological bottlenecks of salmon life histories at sea in time and space. Our study reinforces existing evidence of an impact of early marine growth on maturation decision, with small-sized individuals at the end of the first summer at sea being more likely to delay maturation. However, each population was characterized by a specific probabilistic maturation reaction norm, and a local component of growth at sea in which some populations have better growth in some years might further amplify differences in maturation rate. Differences between populations were smaller than those between sexes, suggesting that the sex-specific growth threshold for maturation is a well-conserved evolutionary phenomenon in salmon. Finally, our results illustrate that although most of the gain in length occurs during the first summer at sea, the temporal variability in body length at return is buffered against the decrease in post-smolt growth conditions. The intricate combination of growth over successive seasons, and its interplay with the maturation decision, could be regulating body length by maintaining diversity in early growth trajectories, life histories, and the composition of salmon populations.     

Impacts of invasive fish removal through angling on population characteristics and juvenile growth rate

Exploitation can modify the characteristics of fish populations through the selective harvesting of individuals, with this potentially leading to rapid ecological and evolutionary changes. Despite the well‐known effects of invasive fishes on aquatic ecosystems generally, the potential effects of their selective removal through angling, a strategy commonly used to manage invasive fish, are poorly understood. The aim of this field‐based study was to use the North American pumpkinseed Lepomis gibbosus as the model species to investigate the consequences of selective removal on their population characteristics and juvenile growth rates across 10 populations in artificial lakes in southern France. We found that the maximal individual mass in populations decreased as removal pressure through angling increased, whereas we did not observed any changes in the maximal individual length in populations as removal pressure increased. Total population abundance did not decrease as removal pressure increased; instead, here was a U‐shaped relationship between removal pressure and the abundance of medium‐bodied individuals. In addition, population biomass had a U‐shaped curve response to removal pressure, implying that invasive fish populations can modulate their characteristics to compensate for the negative effects of selective removals. In addition, individual lengths at age 2 and juvenile growth rates decreased as removal pressure through angling increased, suggesting a shift toward an earlier size at maturity and an overall slower growing phenotype. Therefore, these outputs challenge the efficiency of selective management methods, suggesting the use of more proactive strategies to control invasive populations, and the need to investigate the potential ecological and evolutionary repercussions of nonrandom removal.     

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.     

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.     

Sex-specific life history patterns in bluegill (Lepomis macrochirus): interacting mechanisms influence individual body size

The ultimate body size that an individual fish achieves can be a function both of direct effects of growth or indirect effects associated with the timing of sexual maturation (and associated energetic tradeoffs). These alternatives are often invoked to explain variation in body size within and among fish populations, but have rarely been considered simultaneously. We assessed how resource availability and timing of maturation interact to influence individual body size of bluegill (Lepomis macrochirus). Resource availability (high and low food) and the social structure of the population (presence or absence of large, mature males) were varied in experimental ponds. Food ration affected growth (larger fish in the high food treatments) and the social structure of the population affected timing of maturation (early maturation of males in the absence of large males). Treatment effects, however, were sex-specific; males responded to the social structure of the population and females were more responsive to resource availability. We also found individuals that became sexually mature were smaller than those that remained immature, although results were sex-specific and resource dependent. For males, individuals that matured were smaller when resources were limited; mature and immature females showed no difference in body size regardless of food ration. We show that both resource availability and the processes that control timing of maturation interact in sex-specific ways to influence body size of bluegill. These results suggest that a more robust explanation for variable body size requires consideration of sex-specific interactions between ecological (food and growth) and evolutionary (timing of maturation) mechanisms.     

Adaptive changes in harvested populations: plasticity and evolution of age and size at maturation

We investigate harvest-induced adaptive changes in age and size at maturation by modelling both plastic variation and evolutionary trajectories. Harvesting mature individuals displaces the reaction norm for age and size at maturation toward older ages and larger sizes and rotates it clockwise, whereas harvesting immature individuals has the reverse qualitative effect. If both immature and mature individuals are harvested, the net effect has approximately the same trend as when harvesting immature individuals only. This stems from the sensitivity of the evolutionary response, which depends on the maturity state of harvested individuals, but also on the type of harvest mortality (negatively or positively density dependent, density independent) and the value of three life-history parameters (natural mortality, growth rate and the trade-off between growth and reproduction). Evolutionary changes in the maturation reaction norm have strong repercussions for the mean size and the density of harvested individuals that, in most cases, result in the reduction of biomass--a response that population dynamical models would overlook. These results highlight the importance of accounting for evolutionary trends in the long-term management of exploited living resources and give qualitative insights into how to minimize the detrimental consequences of harvest-induced evolutionary changes in maturation reaction norms.     

Experimental assessment of the probabilistic maturation reaction norm: condition matters

The probabilistic maturation reaction norm (PMRN) describes an individual''s probability of maturing at a given age as a function of size and other relevant phenotypic traits. Population-level shifts in the PMRN are often interpreted to indicate genetic as opposed to phenotypic changes in maturation in fish. Inferences derived from trends in the PMRN have been challenged, warranting an experimental assessment of the method. This was accomplished in a laboratory experiment using zebrafish (Danio rerio). Fish were reared under different food levels to induce variation in growth and maturation. Plasticity in maturation was not entirely captured by the demographic age- and length-based PMRN. Adding condition to the PMRN captured a greater amount of environmental variation in maturation probability. Nevertheless, significant differences in the PMRNs among the food levels remained after accounting for the influences of age, size and condition on maturation probability indicating plasticity of the PMRN. This was particularly pronounced between fish held on low food levels as compared with fish experiencing abundant resources, with the latter experiencing higher size-specific maturation probabilities. Our analysis emphasizes the need for incorporating salient physiological traits influencing maturation, such as condition, to make accurate inferences about documented shifts observed in the position of PMRNs on maturation trends in wild fish stocks.     

Effects of predation environment and food availability on somatic growth in the Livebearing Fish Brachyrhaphis rhabdophora (Pisces: Poeciliidae)

Variation in somatic growth rates is of great interest to biologists because of the relationship between growth and other fitness‐determining traits, and it results from both genetic and environmentally induced variation (i.e. plasticity). Theoretical predictions suggest that mean somatic growth rates and the shape of the reaction norm for growth can be influenced by variation in predator‐induced mortality rates. Few studies have focused on variation in reaction norms for growth in response to resource availability between high‐predation and low‐predation environments. We used juvenile Brachyrhaphis rhabdophora from high‐predation and low‐predation environments to test for variation in mean growth rates and for variation in reaction norms for growth at two levels of food availability in a common‐environment experiment. To test for variation in growth rates in the field, we compared somatic growth rates in juveniles in high‐predation and low‐predation environments. In the common‐environment experiment, mean growth rates did not differ between fish from differing predation environments, but the interaction between predation environment and food level took the form of a crossing reaction norm for both growth in length and mass. Fish from low‐predation environments exhibited no significant difference in growth rate between high and low food treatments. In contrast, fish from high‐predation environments exhibited variation in growth rates between high and low food treatments, with higher food availability resulting in higher growth rates. In the field, individuals in the high‐predation environment grow at a faster rate than those in low‐predation environments at the smallest sizes (comparable to sizes in the common‐environment experiment). These data provide no evidence for evolved differences in mean growth rates between predation environments. However, fish from high‐predation environments exhibited greater plasticity in growth rates in response to resource availability suggesting that predation environments may exhibit increased variation in food availability for prey fish and consequent selection for plasticity.     

HOW TO MEASURE MATURATION: A COMPARISON OF PROBABILISTIC METHODS USED TO TEST FOR GENOTYPIC VARIATION AND PLASTICITY IN THE DECISION TO MATURE

Maturation is a developmental trait that plays a key role in shaping organisms’ life‐history. However, progress in understanding how maturation phenotypes evolve has been held back by confusion over how best to model maturation decisions and a lack of studies comparing genotypic variation in maturation. Here, we fitted probabilistic maturation reaction norms (PMRNs) to data collected from five clones of Daphnia magna and five of Daphnia pulex collected from within and between different populations. We directly compared the utility of modeling approaches that assume maturation to be a process with an instantaneous rate with those that do not by fitting maturation rate and logistic regression models, and emphasize similarities and differences between them. Our results demonstrate that in Daphnia, PMRNs using a logistic regression approach were simpler to use and provided a better fit to the data. The decision to mature was plastic across a range of growth trajectories and dependent upon both body size and age. However, the age effect was stronger in D. magna than D. pulex and varied considerably between clones. Our results support the idea that maturation thresholds can evolve but also suggest that the notion of a threshold based on a single fixed state is an oversimplification that underestimates the adaptability of these important traits.     

Intraspecific variation in the growth and survival of juvenile fish exposed to Eucalyptus leachate

Whilst changes in freshwater assemblages along gradients of environmental stress have been relatively well studied, we know far less about intraspecific variation to these same stressors. A stressor common in fresh waters worldwide is leachates from terrestrial plants. Leachates alter the physiochemical environment of fresh waters by lowering pH and dissolved oxygen and also releasing toxic compounds such as polyphenols and tannins, all of which can be detrimental to aquatic organisms. We investigated how chronic exposure to Eucalyptus leaf leachate affected the growth and survival of juvenile southern pygmy perch (Nannoperca australis) collected from three populations with different litter inputs, hydrology and observed leachate concentrations. Chronic exposure to elevated leachate levels negatively impacted growth and survival, but the magnitude of these lethal and sublethal responses was conditional on body size and source population. Bigger fish had increased survival at high leachate levels but overall slower growth rates. Body size also varied among populations and fish from the population exposed to the lowest natural leachate concentrations had the highest average stress tolerance. Significant intraspecific variation in both growth and survival caused by Eucalyptus leachate exposure indicates that the magnitude (but not direction) of these stress responses varies across the landscape. This raises the potential for leachate‐induced selection to operate at an among‐population scale. The importance of body size demonstrates that the timing of leachate exposure during ontogeny is central in determining the magnitude of biological response, with early life stages being most vulnerable. Overall, we demonstrate that Eucalyptus leachates are prevalent and potent selective agents that can trigger important sublethal impacts, beyond those associated with more familiar fish kills, and reiterate that dissolved organic carbon is more than just an energy source in aquatic environments.     

Selection for life‐history traits to maximize population growth in an invasive marine species

Species establishing outside their natural range, negatively impacting local ecosystems, are of increasing global concern. They often display life‐history features characteristic for r‐selected populations with fast growth and high reproduction rates to achieve positive population growth rates (r) in invaded habitats. Here, we demonstrate substantially earlier maturation at a 2 orders of magnitude lower body mass at first reproduction in invasive compared to native populations of the comb jelly Mnemiopsis leidyi. Empirical results are corroborated by a theoretical model for competing life‐history traits that predicts maturation at the smallest possible size to optimize r, while individual lifetime reproductive success (R₀), optimized in native populations, is near constant over a large range of intermediate maturation sizes. We suggest that high variability in reproductive tactics in native populations is an underappreciated determinant of invasiveness, acting as substrate upon which selection can act during the invasion process.     

Evolutionary divergence in life history traits among populations of the Lake Malawi cichlid fish Astatotilapia calliptera

During the early stages of adaptive radiation, populations diverge in life history traits such as egg size and growth rates, in addition to eco‐morphological and behavioral characteristics. However, there are few studies of life history divergence within ongoing adaptive radiations. Here, we studied Astatotilapia calliptera, a maternal mouthbrooding cichlid fish within the Lake Malawi haplochromine radiation. This species occupies a rich diversity of habitats, including the main body of Lake Malawi, as well as peripheral rivers and shallow lakes. We used common garden experiments to test for life history divergence among populations, focussing on clutch size, duration of incubation, egg mass, offspring size, and growth rates. In a first experiment, we found significant differences among populations in average clutch size and egg mass, and larger clutches were associated with smaller eggs. In a second experiment, we found significant differences among populations in brood size, duration of incubation, juvenile length when released, and growth rates. Larger broods were associated with smaller juveniles when released and shorter incubation times. Although juvenile growth rates differed between populations, these were not strongly related to initial size on release. Overall, differences in life history characters among populations were not predicted by major habitat classifications (Lake Malawi or peripheral habitats) or population genetic divergence (microsatellite‐based F_ST). We suggest that the observed patterns are consistent with local selective forces driving the observed patterns of trait divergence. The results provide strong evidence of evolutionary divergence and covariance of life history traits among populations within a radiating cichlid species, highlighting opportunities for further work to identify the processes driving the observed divergence.     

Life history plasticity in the satyrine butterfly Lasiommata petropolitana: investigating an adaptive reaction norm

This study addresses the general hypothesis that insects living in seasonal environments should shorten development times at progressively later dates in the growth season, and that insects living outside equatorial areas should use daylength as a cue to determine the date. Diapause strategies and reaction norms relating the duration of larval development to daylength was investigated in a French population of the butterfly, Lasiommata petropolitana. The results are compared with those of an earlier study of the species in Sweden. Because of the diapausing strategy and phenology of the population, it was expected that an adaptive reaction norm relating larval time to daylength should have a positive slope, i.e. relatively shorter daylengths induce faster growth and development. This prediction was supported, and the reaction norm was qualitatively similar to the one found in Swedish populations. In the French population it was, however, shifted to a range of shorter photoperiods which corresponds to the regime of shorter daylengths in southern Europe. Shorter larval development times and high growth rates were associated with a reduction in pupal size, suggesting a trade off between time and size at pupation. There was no evidence of a trade off between growth rate and starvation endurance. The results suggests that the daylength-dependent decision of what growth trajectory an individual larva will follow, is not made continuously but rather at one or a few occasions during larval development. It is clear that larvae of L. petropolitana make developmental decisions in relation to the daylength they experience during larval growth. The result is a reaction norm that agrees closely to what is predicted by some life history models, suggesting that it is an adaptation for optimising life history traits in a seasonal environment.