Maturation Reaction Norms Research Articles

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.

The reaction norm of size and age at maturity under multiple predator risk

1. Two major theories underpin our understanding of how predation risk shapes life history. The first is centred around predator induced changes in activity that subsequently reduce food intake and thus growth. The second is centred around size selective, predator induced changes in development. 2. Here, we challenge these theories using experiments and probabilistic models of maturation reaction norms to investigate predator induced life history in the water flea Daphnia pulex facing two different predators. 3. We combine this reaction norm investigation with an assessment of growth rate, development rate, moult number and moult duration to uncover the mechanisms controlling predator induced life history plasticity when D. pulex face either large or small size selective predators. 4. The probabilistic reaction norms reveal predator specific norms of reaction in size and age along a food gradient. Fish cues reduce age and size, with a bias in age, and do so by reducing moult number and duration. Midge cues increase age and size, with a bias in size, and do so by fine scale modulation of early growth rates. 5. These data contribute towards developing a unified view of how predation risk from multiple predators shapes life history evolution.

General Classification of Maturation Reaction-Norm Shape from Size-based Processes

Phenotypic plasticity of size at maturation is commonly described using size-age maturation reaction norms (MRNs). MRNs for age and size at maturation are analyzed and classified into three general categories related to different size scalings of growth and mortality. The underlying model for growth and mortality is based on processes at the level of the individual, and is motivated by the energy budget of fish. MRN shape is a balance between opposing factors and depends on subtle details of size dependence of growth and mortality. MRNs with both positive and negative slopes are predicted, and for certain mortality conditions also a lower critical spawning mass. The model is applied to predict a generic fishery-induced evolutionary response and allows assessment of climate change impact on MRNs. Our work stresses the importance of using realistic size dependence of mortality and growth, since this strongly influences the predicted MRNs and sensitivity to harvest pressure.

Maturation Schedules of Walleye Populations in the Great Lakes Region: Comparison of Maturation Indices and Evaluation of Sampling‐Induced Biases

AbstractMaturation schedules, key determinants of fish stocks' harvest potential and population dynamics, are influenced by both plastic and adaptive processes. Various indices are used to describe maturation schedules, and these have differential advantages for discriminating between plastic and adaptive processes. However, potential sampling‐related biases associated with different maturation indices have not been fully evaluated. We analyzed three maturation indices for walleyes Sander vitreus in Lake Erie; Saginaw Bay, Lake Huron; and Oneida Lake, New York: age and length at 50% maturity, midpoint of age‐specific maturity ogives (age‐specific length at which probability of maturity = 0.50), and midpoints of probabilistic maturation reaction norms (PMRNs; age‐specific length at which probability of maturing in the following year = 0.50). We then compared estimated maturation indices to evaluate sensitivity of different maturation indices to sampling‐induced biases and to assess the relative importance of plastic versus adaptive processes in structuring interstock and temporal variation in maturation schedules. Our findings suggest that although small changes in sampling month, gear, and agency‐related effects can bias estimates of age and length at 50% maturity and midpoints of maturity ogives, PMRN estimates appear to be robust to these biases. Furthermore, PMRN estimates are suggestive of potential adaptive variation in maturation schedules among walleye stocks and over time. For instance, Oneida Lake walleyes (which had relatively slow growth and low mortality rates) matured at a smaller size for a given age (smaller midpoints of PMRNs) than the other stocks. Temporally, walleyes in the western basin of Lake Erie matured at a larger size in recent years, as evidenced by increasing midpoints of PMRNs (1978–1989 versus 1990–2006 for Ohio Department of Natural Resources data and 1990–1996 versus 1997–2006 for Ontario Ministry of Natural Resources data). Our study highlights the necessity of monitoring maturation schedules via multiple maturation indices and the need to account for sampling‐induced biases when comparing maturation schedules.

Temporal trends in probabilistic maturation reaction norms and growth of Atlantic cod (Gadus morhua) on the Icelandic shelf

Decreasing temporal trends in probabilistic maturation reaction norm (PMRN) midpoints, symptomatic of earlier maturation despite environmentally induced variation in growth, have been observed in many exploited fish stocks. Here, we studied the growth and maturation trends of female and male Icelandic cod ( Gadus morhua ) by estimating PMRN midpoints for cohorts 1964–1999 and found evidence that a shift towards maturation at smaller sizes and younger ages has occurred independently of changes in growth, condition, and temperature. Weighting the data with regional survey abundance estimates to account for spatial heterogeneity in maturity status and sampling intensity did not qualitatively affect the temporal trends. Length-at-age also decreased through the study period, which, through simulations, could be attributed to the energetic costs of earlier maturity at maturing age groups but not at younger ages. These findings support the hypothesis that such changes in maturation schedules are not caused by environmental factors alone but could also reflect a genetic change, potentially in response to intensive fishing.

EDITORIAL: Toward Darwinian fisheries management

There is increasing evidence that fishing may cause rapid contemporary evolution in freshwater and marine fish populations. This has led to growing concern about the possible consequences such evolutionary change might have for aquatic ecosystems and the utility of those ecosystems to society. This special issue contains contributions from a symposium on fisheries-induced evolution held at the American Fisheries Society Annual Meeting in August 2008. Contributions include primary studies and reviews of field-based and experimental evidence, and several theoretical modeling studies advancing life-history theory and investigating potential management options. In this introduction we review the state of research in the field, discuss current controversies, and identify contributions made by the papers in this issue to the knowledge of fisheries-induced evolution. We end by suggesting directions for future research.

Eco-genetic model to explore fishing-induced ecological and evolutionary effects on growth and maturation schedules.

Eco-genetic individual-based models involve tracking the ecological dynamics of simulated individual organisms that are in part characterized by heritable parameters. We developed an eco-genetic individual-based model to explore ecological and evolutionary interactions of fish growth and maturation schedules. Our model is flexible and allows for exploration of the effects of heritable growth rates (based on von Bertalanffy and biphasic growth patterns), heritable maturation schedules (based on maturation reaction norm concepts), or both on individual- and population-level traits. In baseline simulations with rather simple ecological trade-offs and over a relatively short time period (<200 simulation years), simulated male and female fish evolve differential genetic growth and maturation. Further, resulting patterns of genetically determined growth and maturation are influenced by mortality rate and density-dependent processes, and maturation and growth parameters interact to mediate the evolution of one another. Subsequent to baseline simulations, we conducted experimental simulations to mimic fisheries harvest with two size-limits (targeting large or small fish), an array of fishing mortality rates, and assuming a deterministic or stochastic environment. Our results suggest that fishing with either size-limit may induce considerable changes in life-history trait expression (maturation schedules and growth rates), recruitment, and population abundance and structure. However, targeting large fish would cause more adverse genetic effects and may lead to a population less resilient to environmental stochasticity.

ORIGINAL ARTICLE: Comparison of demographic and direct methods to calculate probabilistic maturation reaction norms for Flemish Cap cod (Gadus morhua)

Age and length at maturation have declined in many fish populations and this has been hypothesized to be a genetic change caused by high fishing mortality. Probabilistic Maturation Reaction Norms (PMRNs) have been used as a tool to gain a better understanding of the possible genetic nature of these changes. The demographic and direct methods are two ways to calculate PMRNs. The data requirements are more often met for the demographic method than for the direct method which requires the identification of recruit spawners. However, the demographic method relies on more assumptions than the direct method, typically assuming equality of growth and mortality rates for immature and mature individuals within an age class. This study provides the first direct comparison of demographic and direct methods and shows that both methods produce comparable results. Differences between methods are hypothesized to be owed to possible differences in growth rate between mature and immature individuals in Flemish Cap cod.

Life history change in commercially exploited fish stocks: an analysis of trends across studies.

Age and size at maturation have declined dramatically in many commercial fish stocks over the past few decades – changes that have been widely attributed to fishing pressure. We performed an analysis of such trends across multiple studies, to test for the consistency of life history changes under fishing, and for their association with the intensity of exploitation (fishing mortality rate). We analyzed 143 time series from 37 commercial fish stocks, the majority of which originated from the North Atlantic. Rates of phenotypic change were calculated for two traditional maturation indices (length and age at 50% maturity), as well as for probabilistic maturation reaction norms (PMRNs). We found that all three indices declined in heavily exploited populations, and at a rate that was strongly correlated with the intensity of fishing (for length at 50% maturity and PMRNs). These results support previous assertions that fishing pressure is playing a major role in the life history changes observed in commercial fish stocks. Rates of change were as strong for PMRNs as for age and size at 50% maturity, which is consistent with the hypothesis that fishing-induced phenotypic changes can sometimes have a genetic basis.

Fisheries-induced evolution in growth, maturation and reproductive investment of the sexually dimorphic North Sea plaice ( Pleuronectes platessa L.)

Changes in the onset of sexual maturation, reproductive investment and growth of North Sea plaice are studied between three periods: 1900s, 1980s and 2000s. Probabilistic maturation reaction norms of both males and females, describing the probability of becoming mature conditional on age and size, shifted towards smaller sizes and younger ages, indicating a fisheries-induced evolutionary change. A higher rate of change was observed during the past 20 years, which may be related to higher temperature conditions. Reproductive investment was estimated from the decrease in lipid, protein, dry weight content and condition factor of the whole body between pre- and post-spawning adults. Reproductive investment expressed as the energy loss over the spawning period increased with body size from 19% at 20 cm to 30% at 40 cm in males and from 35% at 30 cm to 48% at 50 cm in females. No change in reproductive investment could be detected between the 1980s and the 2000s. Von Bertalanffy (VB) growth parameters showed a decrease in L ∞ the asymptotic size and an increase in K, the velocity to reach L ∞, in both males and females. The changes in VB growth are consistent with an increase in energy acquisition and reproductive investment. The observed changes in maturation, reproductive investment and growth are consistent with fisheries-induced evolution, but the changes in reproductive investment and growth need further investigation to disentangle the role of phenotypic plasticity.

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.

Intense Habitat-Specific Fisheries-Induced Selection at the Molecular Pan I Locus Predicts Imminent Collapse of a Major Cod Fishery

Predation is a powerful agent in the ecology and evolution of predator and prey. Prey may select multiple habitats whereby different genotypes prefer different habitats. If the predator is also habitat-specific the prey may evolve different habitat occupancy. Drastic changes can occur in the relation of the predator to the evolved prey. Fisheries exert powerful predation and can be a potent evolutionary force. Fisheries-induced selection can lead to phenotypic changes that influence the collapse and recovery of the fishery. However, heritability of the phenotypic traits involved and selection intensities are low suggesting that fisheries-induced evolution occurs at moderate rates at decadal time scales. The Pantophysin I (Pan I) locus in Atlantic cod (Gadus morhua), representing an ancient balanced polymorphism predating the split of cod and its sister species, is under an unusual mix of balancing and directional selection including current selective sweeps. Here we show that Pan I alleles are highly correlated with depth with a gradient of 0.44% allele frequency change per meter. AA fish are shallow-water and BB deep-water adapted in accordance with behavioral studies using data storage tags showing habitat selection by Pan I genotype. AB fish are somewhat intermediate although closer to AA. Furthermore, using a sampling design covering space and time we detect intense habitat-specific fisheries-induced selection against the shallow-water adapted fish with an average 8% allele frequency change per year within year class. Genotypic fitness estimates (0.08, 0.27, 1.00 of AA, AB, and BB respectively) predict rapid disappearance of shallow-water adapted fish. Ecological and evolutionary time scales, therefore, are congruent. We hypothesize a potential collapse of the fishery. We find that probabilistic maturation reaction norms for Atlantic cod at Iceland show declining length and age at maturing comparable to changes that preceded the collapse of northern cod at Newfoundland, further supporting the hypothesis. We speculate that immediate establishment of large no-take reserves may help avert collapse.

Spatial variation in growth, condition and maturation reaction norms of the Baltic herring Clupea harengus membras

Understanding of spatial patterns in life-history traits can help fisheries management focus on biologically and functionally relevant stock units. In the present study, we examined life-history variation in growth, condition and maturation of the Baltic herring Clupea harengus membras among different areas of the Baltic Sea. As expected based on environmental gradients, herring grew faster in southern than in northern areas. The condition factor for young individuals was higher in the north, but higher for older individuals in the south. Probabilistic maturation reaction norms (PMRNs) based on age, length and condition indicated counter-gradient variation: young herring in the northern areas reached the size at which they had a 50% probability of maturing when they were comparatively smaller than the southern specimens. However, the north-south differences in PMRNs were reversed in older age groups. This indicated that maturation of herring in the north was more size dependent (zero PMRN slope) than it was for herring in the south, where maturation was predominantly determined by age (negative PMRN slope). The geographical differentiation in maturation schedules would potentially translated into divergent changes in recruitment in response to changes in density-dependent growth and, hence, also fishing patterns.

Two- and three-dimensional maturation reaction norms for the eastern Baltic cod, Gadus morhua

Abstract Vainikka, A., Gårdmark, A., Bland, B., and Hjelm, J. 2009. Two- and three-dimensional maturation reaction norms for the eastern Baltic cod, Gadus morhua. – ICES Journal of Marine Science, 66: 248–257. Industrial fisheries have caused decreases in the size and age at maturation in several stocks of cod (Gadus morhua). Although earlier maturation can be a phenotypic response to improved growth conditions, estimation of probabilistic maturation reaction norms (PMRNs) can remove most impacts of growth and demography from maturation schedules and has often revealed a residual, potentially genetic, trend. In this study, size- and condition-based PMRNs were estimated for eastern Baltic cod cohorts from 1987 to 2003. The PMRNs suggested that both length and condition at 50% probability of maturing (Lp50 and Cp50) had decreased by 15–20%, more notably in females. Simultaneously with changes in maturation schedules, the length-at-age of mature fish decreased for most combinations of age and sex. Decrease in growth may be partly explained by advanced maturation, but temporal fluctuations in PMRNs suggest also a residual environmental impact on both growth and maturation. The results may indicate a genetic change in the eastern Baltic cod stock, adding pressure to reduce fishing mortality on it.

Spatial and temporal variation of maturation schedules of lake whitefish (Coregonus clupeaformis) in the Great Lakes

Fish maturation schedules vary greatly among systems and over time, reflecting both plastic and adaptive responses to ecosystem structure, physical habitats, and mortality (natural and fishing). We examined maturation schedules of commercially exploited lake whitefish ( Coregonus clupeaformis ) in the Laurentian Great Lakes (Lakes Michigan, Huron, and Superior) by estimating ages and lengths at 50% maturity, age-specific maturity ogives (age-specific probability of being mature), and probabilistic maturation reaction norms (PMRNs; a metric that accounts for effects of growth and mortality). Collectively, these estimates indicated variation in maturation schedules between sexes (i.e., males tend to mature at younger ages and shorter lengths than females) and among systems (midpoint estimates of PMRNs were smallest for Lake Michigan fish, intermediate for fish in the main basin of Lake Huron, and largest for fish in Lake Huron’s Georgian Bay and Lake Superior). Temporally, recent increases in age at 50% maturity in Lakes Huron and Michigan may primarily reflect plastic responses to decreased growth rates associated with ecosystem changes (e.g., declines of the native amphipod, Diporeia spp.). As plastic and adaptive changes in maturation schedules of fish stocks may occur simultaneously and require different management considerations, we recommend the concomitant analysis of multiple maturation indices.

Small-scale biocomplexity in coastal Atlantic cod supporting a Darwinian perspective on fisheries management.

Harvesting of marine resources raises concerns about how to identify and preserve biocomplexity, including the diversity of life histories found within and among wild populations of a species. In order to fully accomplish this, there is a need to elucidate the underlying causes of phenotypic variation, and how this variation responds to environmental changes. In general, both evolutionary (genetic) and nonevolutionary (plastic) responses may occur. Plastic responses to environmental change are expected to shift the phenotype along a reaction norm, while an evolutionary response is expected to shift the reaction norm itself. Here, we assess the maturation patterns of coastal Atlantic cod (Gadus morhua) in Skagerrak, where studies using neutral markers have revealed genetically differentiated populations of this harvested fish within tens of kilometres of coastline. Our results suggest that physiological state prior to the spawning season, as well as juvenile growth, both influence the probability of completing sexual maturation at a given age. Furthermore, our results point towards a spatial structuring of this plasticity (i.e. the maturation reaction norms) comparable with population connectivity inferred from neutral markers. We argue that such fine-scale biocomplexity calls for a Darwinian approach to fisheries management.

The role of growth history in determining age and size at maturation in exploited fish populations

AbstractRecently, a great deal of attention has been focused on investigating whether decreased ages and sizes at maturation in exploited fish populations could be evolutionary responses to selective fishing. To this end, the main focus has been on isolating the effects of growth changes from the process of maturation, but little effort has been invested in assessing how growth actually affects ages and sizes at maturation in a population. Here, we develop a probabilistic description of the process of maturation, which makes explicit the mathematical links between maturation, growth and the probabilistic maturation reaction norm. Apart from providing a mathematically explicit yet heuristically simple framework for assessing the role of growth in the age and size at maturation, we demonstrate by simulation that changes in growth rates can result in considerable shifts in the age and size at maturation. Focusing more attention on growth histories of individuals would provide a better position to understand the processes constituting phenotypic shifts in the age and size at maturation and help in disentangling environmentally induced plastic changes in maturation from those caused by evolutionary responses to fisheries‐induced selection.

Evolution of growth in Gulf of St Lawrence cod?

Fishing is often size selective such that the likelihood of capture increases with body size. It has therefore been postulated that fishing could favour evolution of slower growth because smaller size would reduce exposure to fishing gear (e.g. [Ricker 1981][1]). A recent study by Swain et al . ([

Fisheries-induced evolutionary changes in maturation reaction norms in North Sea sole Solea solea

Age and size at maturation decreased in several commercially exploited fish stocks, which, according to life history theory, may be due to fisheries-induced evolutionary change. How- ever, the observed changes may also represent a plastic response to environmental variability. To dis- entangle phenotypic plasticity from evolutionary change, the probabilistic reaction norm approach was applied to 43 cohorts (1960 to 2002) of female sole Solea solea from market samples. The reaction norm for age and size at first maturation has significantly shifted towards younger age and smaller size. Size at 50% probability of maturation at Age 3 decreased from 28.6 cm (251 g) to 24.6 cm (128 g). This change was even stronger when condition was included as a third dimension in the reaction norm estimation. The influence of alternative factors was tested on the population level by regression of reaction norm midpoints on annual estimates of condition, temperature and competitive biomass. Although effects of temperature and competitive biomass were significant, the variation in the midpoints was best explained by the decreasing time trend. Therefore, the results provide strong evidence for a fisheries-induced evolutionary change in the onset of sexual maturity.

Demographic and Evolutionary Consequences of Selective Mortality: Predictions from an Eco‐Genetic Model for Smallmouth Bass

AbstractWe use an individual‐based eco‐genetic model to examine the demographic and evolutionary consequences of selective mortality on a species with parental care, the smallmouth bass Micropterus dolomieu. Our analyses are grounded in a long‐term (1936‐2003) empirical study of the dynamics of two populations that differ widely in both density and life history. The model we construct extends previous approaches by including phenotypic plasticity in age and size at maturation, by permitting density‐dependent somatic growth, and by analyzing how costs associated with parental care alter model predictions. We show that, first, additional mortality on age‐0 individuals applied for 100 years causes reduced population abundance and biomass, faster somatic growth rates, and phenotypic plasticity toward slightly larger sizes at maturation. Second, mortality on individuals above a minimum size limit, also applied for 100 years, has a small influence on population abundance and somatic growth, causes a reduction of biomass, and substantial evolution of the probabilistic maturation reaction norm, leading to younger ages and smaller sizes at maturation. Third, the incorporation of body‐size‐dependent survival costs associated with parental care (i.e., by reducing the number of small breeding adults at high population densities, increasing the mortality of parents that breed at small body sizes, or increasing the mortality of offspring originating from small‐sized parents) reduces the amount of evolution predicted to occur within 100 years. Together, these results underscore that selective harvest can cause both phenotypically plastic responses and rapid evolution; however, the rate and magnitude of the evolved changes are sensitive to a species' life history characteristics.