EVOLUTION OF GIGANTISM IN NINE‐SPINED STICKLEBACKS

The relaxation of predation and interspecific competition are hypothesized to allow evolution toward “optimal” body size in island environments, resulting in the gigantism of small organisms. We tested this hypothesis by studying a small teleost (nine‐spined stickleback, Pungitius pungitius) from four marine and five lake (diverse fish community) and nine pond (impoverished fish community) populations. In line with theory, pond fish tended to be larger than their marine or lake conspecifics, sometimes reaching giant sizes. In two geographically independent cases when predatory fish had been introduced into ponds, fish were smaller than those in nearby ponds lacking predators. Pond fish were also smaller when found in sympatry with three‐spined stickleback (Gasterosteus aculeatus) than those in ponds lacking competitors. Size‐at‐age analyses demonstrated that larger size in ponds was achieved by both increased growth rates and extended longevity of pond fish. Results from a common garden experiment indicate that the growth differences had a genetic basis: pond fish developed two to three times higher body mass than marine fish during 36 weeks of growth under similar conditions. Hence, reduced risk of predation and interspecific competition appear to be chief forces driving insular body size evolution toward gigantism.     

Contrasting growth strategies of pond versus marine populations of nine-spined stickleback (Pungitius pungitius): a combined effect of predation and competition?

Gigantism in isolated ponds in the absence of sympatric fish species has previously been observed in nine-spined sticklebacks (Pungitius pungitius). Patterns in sexual size dimorphism suggested that fecundity selection acting on females might be responsible for the phenomenon. However, the growth strategy behind gigantism in pond sticklebacks has not been studied yet. Here, we compared von Bertalanffy growth parameters of four independent nine-spined stickleback populations reared in a common laboratory environment: two coastal marine (typical size) and two pond (giant size) populations. We found that both pond populations had larger estimated final size than marine populations, which in turn exhibited higher intrinsic growth rates than the pond populations. Female growth strategies were more divergent among marine and pond populations than those of males. Asymptotic body size and intrinsic growth rate were strongly negatively correlated. Hence, pond versus marine populations exhibited different growth strategies along a continuum. Our data suggest that quick maturation—even with the cost of being small (low fecundity)—is favoured in marine environments. On the contrary, growth to a giant final size (high fecundity)—even if it entails extended growth period—is favoured in ponds. We suggest that the absence (ponds) versus presence (marine environment) of sympatric predatory fish species, and the consequent change in the importance of intraspecific competition are responsible for the divergence in growth strategies. The sex-dependence of the patterns further emphasizes the role of females in the body size divergence in the species. Possible alternative hypotheses are also discussed.     

Body size divergence in nine‐spined sticklebacks: disentangling additive genetic and maternal effects

Interpopulation differences in body size are of common occurrence in vertebrates, but the relative importance of genetic, maternal, and environmental effects as causes of observed differentiation have seldom been assessed in the wild. Gigantism in pond nine‐spined sticklebacks (Pungitius pungitius Linnaeus, 1758) has been repeatedly observed, but the quantitative genetic basis of population divergence in size has remained unstudied. We conducted a common garden experiment – using ‘pure’ and reciprocal crosses between two populations (‘giant’ pond versus ‘normal’ marine) – to test for the relative importance of additive genetic, non‐additive genetic, and maternal effects on body size after 11 months of growth in the laboratory. We found that body size difference between the two populations in laboratory conditions owed mainly to additive genetic effects, and only to a minor degree to maternal effects. Furthermore, the weak maternal effects were seen only in the offspring of ‘giant’ mothers, and appeared to be mediated through differences in egg size. Thus, the results suggest that gigantism in pond populations of P. pungitius is based on the effects of additively acting genes, rather than to direct environmental induction, or maternal or non‐additive gene action. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 521–528.     

A century of fish growth in relation to climate change,population dynamics and exploitation

Marine ecosystems, particularly in high‐latitude regions such as the Arctic, have been significantly affected by human activities and contributions to climate change. Evaluating how fish populations responded to past changes in their environment is helpful for evaluating their future patterns, but is often hindered by the lack of long‐term biological data available. Using otolith increments of Northeast Arctic cod (Gadus morhua) as a proxy for individual growth, we developed a century‐scale biochronology (1924–2014) based on the measurements of 3,894 fish, which revealed significant variations in cod growth over the last 91 years. We combined mixed‐effect modeling and path analysis to relate these growth variations to selected climate, population and fishing‐related factors. Cod growth was negatively related to cod population size and positively related to capelin population size, one of the most important prey items. This suggests that density‐dependent effects are the main source of growth variability due to competition for resources and cannibalism. Growth was also positively correlated with warming sea temperatures but negatively correlated with the Atlantic Multidecadal Oscillation, suggesting contrasting effects of climate warming at different spatial scales. Fishing pressure had a significant but weak negative direct impact on growth. Additionally, path analysis revealed that the selected growth factors were interrelated. Capelin biomass was positively related to sea temperature and negatively influenced by herring biomass, while cod biomass was mainly driven by fishing mortality. Together, these results give a better understanding of how multiple interacting factors have shaped cod growth throughout a century, both directly and indirectly.     

Evidence for genetic differentiation in timing of maturation among nine‐spined stickleback populations

Timing of maturation is an important life‐history trait that is likely to be subjected to strong natural selection. Although population differences in timing of maturation have been frequently reported in studies of wild animal populations, little is known about the genetic basis of this differentiation. Here, we investigated population and sex differences in timing of maturation within and between two nine‐spined stickleback (Pungitius pungitius) populations in a laboratory breeding experiment. We found that fish from the high‐predation marine population matured earlier than fish from the low‐predation pond population and males matured earlier than females. Timing of maturation in both reciprocal hybrid crosses between the two populations was similar to that in the marine population, suggesting that early timing of maturation is a dominant trait, whereas delayed timing of maturation in the pond is a recessive trait. Thus, the observed population divergence is suggestive of strong natural selection against early maturation in the piscine‐predator‐free pond population.     

Morphological divergence of North‐European nine‐spined sticklebacks (Pungitius pungitius): signatures of parallel evolution

Parallel evolution is characterised by repeated, independent occurrences of similar phenotypes in a given habitat type, in different parts of the species distribution area. We studied body shape and body armour divergence between five marine, four lake, and ten pond populations of nine‐spined sticklebacks [Pungitius pungitius (Linnaeus, 1758)] in Fennoscandia. We hypothesized that marine and lake populations (large water bodies, diverse fish fauna) would be similar, whereas sticklebacks in isolated ponds (small water bodies, simple fish fauna) would be divergent. We found that pond fish had deeper bodies, shorter caudal peduncles, and less body armour (viz. shorter/absent pelvic spines, reduced/absent pelvic girdle, and reduced number of lateral plates) than marine fish. Lake fish were intermediate, but more similar to marine than to pond fish. Results of our common garden experiment concurred with these patterns, suggesting a genetic basis for the observed divergence. We also found large variation among populations within habitat types, indicating that environmental variables other than those related to gross habitat characteristics might also influence nine‐spined stickleback morphology. Apart from suggesting parallel evolution of morphological characteristics of nine‐spined sticklebacks in different habitats, the results also show a number of similarities to the evolution of three‐spined stickleback (Gasterosteus aculeatus Linnaeus, 1758) morphology. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 403–416.     

Population divergence in compensatory growth responses and their costs in sticklebacks

Compensatory growth (CG) may be an adaptive mechanism that helps to restore an organisms’ growth trajectory and adult size from deviations caused by early life resource limitation. Yet, few studies have investigated the genetic basis of CG potential and existence of genetically based population differentiation in CG potential. We studied population differentiation, genetic basis, and costs of CG potential in nine‐spined sticklebacks (Pungitius pungitius) differing in their normal growth patterns. As selection favors large body size in pond and small body size in marine populations, we expected CG to occur in the pond but not in the marine population. By manipulating feeding conditions (viz. high, low and recovery feeding treatments), we found clear evidence for CG in the pond but not in the marine population, as well as evidence for catch‐up growth (i.e., size compensation without growth acceleration) in both populations. In the marine population, overcompensation occurred individuals from the recovery treatment grew eventually larger than those from the high feeding treatment. In both populations, the recovery feeding treatment reduced maturation probability. The recovery feeding treatment also reduced survival probability in the marine but not in the pond population. Analysis of interpopulation hybrids further suggested that both genetic and maternal effects contributed to the population differences in CG. Hence, apart from demonstrating intrinsic costs for recovery growth, both genetic and maternal effects were identified to be important modulators of CG responses. The results provide an evidence for adaptive differentiation in recovery growth potential.     

Adaptive brain size divergence in nine‐spined sticklebacks (Pungitius pungitius)?

Most studies seeking to provide evolutionary explanations for brain size variability have relied on interspecific comparisons, while intraspecific studies utilizing ecologically divergent populations to this effect are rare. We investigated the brain size and structure of first‐generation laboratory‐bred nine‐spined sticklebacks (Pungitius pungitius) from four geographically and genetically isolated populations originating from markedly different habitats. We found that the relative size of bulbus olfactorius and telencephalon was significantly larger in marine than in pond populations. Significant, but habitat‐independent population differences were also found in relative brain and cerebellum sizes. The consistent, habitat‐specific differences in the relative size of bulbus olfactorius and telencephalon suggest their adaptive reduction in response to reduced (biotic and abiotic) habitat complexity in pond environments. In general, the results suggest that genetically based brain size and structure differences can evolve relatively rapidly and in repeatable fashion with respect to habitat structure.     

Effects of the sea louse Lepeophtheirus salmonis on temporal changes in cortisol,sex steroids,growth and reproductive investment in Arctic charr Salvelinus alpinus

Groups of mature (5+ year old) Arctic charr Salvelinus alpinus held in sea water were exposed for 34 days to either a high (mean ±s.e . 0·15 ± 0·01 sea lice Lepeophtheirus salmonis g^?1 fish mass) (HI), medium (0·07 ± 0·00 sea lice g^?1 fish mass) (MI) or no [control (C)] sea‐lice infection during early stages of gonad development (June to July). Infection with sea lice resulted in increased plasma cortisol concentrations and this was related to intensity of infection; females tended to have higher cortisol concentrations than males at high infection intensities (HI group: female c. 130 ng ml^?1; male c. 80 ng ml^?1). Plasma osmolality (C c. 330, MI c. 350 and HI c. 415 mOsm) and chloride concentrations (C c. 135, MI c. 155 and HI c. 190 mM) increased significantly with infection intensity, indicating osmoregulatory problems in infected fish. A strong positive relationship between plasma osmolality and cortisol concentration was recorded. Plasma sex‐steroid concentrations were influenced negatively by sea‐lice infection, particularly in the HI group, and were inversely related to plasma cortisol concentrations. The most heavily infected fish postponed the initiation of reproductive development until exposed to fresh water and timing of ovulation tended to be delayed in these fish. Growth rate and condition were negatively influenced by sea‐lice infection and growth rate was inversely related to plasma cortisol concentrations. Sea‐lice infection resulted in mortality among females in the HI group, and the proportion of maturing females was lower in the MI group (46%) than in the controls (85%). Egg production in the MI and HI groups was c. 50 and 30% of the C group. Egg size, embryonic survival and fry mass did not differ across groups. Sea lice influence reproductive development and egg production in S. alpinus, and consequently these parasites may influence populations via sublethal effects on broodfish, affecting growth and condition, and their reproductive output.     

Influences of multilocus heterozygosity on size during early life

Genetic diversity has been hypothesized to promote fitness of individuals and populations, but few studies have examined how genetic diversity varies with ontogeny. We examined patterns in population and individual genetic diversity and the effect of genetic diversity on individual fitness among life stages (adults and juveniles) and populations of captive yellow perch (Perca flavescens) stocked into two ponds and allowed to spawn naturally. Significant genetic structure developed between adults and offspring in a single generation, even as heterozygosity and allelic richness remained relatively constant. Heterozygosity had no effect on adult growth or survival, but was significantly and consistently positively related to offspring length throughout the first year of life in one pond but not the other. The largest individuals in the pond exhibiting this positive relationship were more outbred than averaged size individuals and also more closely related to one another than they were to average‐sized individuals, suggesting potential heritability of body size or spawn timing effects. These results indicate that the influence of heterozygosity may be mediated through an interaction, likely viability selection, between ontogeny and environment that is most important during early life. In addition, populations may experience significant genetic change within a single generation in captive environments, even when allowed to reproduce naturally. Accounting for the dynamic influences of genetic diversity on early life fitness could lead to improved understanding of recruitment and population dynamics in both wild and captive populations.     

Life history constraints explain negative relationship between fish productivity and dissolved organic carbon in lakes

Resource availability constrains the life history strategies available to organisms and may thereby limit population growth rates and productivity. We used this conceptual framework to explore the mechanisms driving recently reported negative relationships between fish productivity and dissolved organic carbon (DOC) concentrations in lakes. We studied populations of bluegill (Lepomis macrochirus) in a set of lakes with DOC concentrations ranging from 3 to 24 mg/L; previous work has demonstrated that primary and secondary productivity of food webs is negatively related to DOC concentration across this gradient. For each population, we quantified individual growth rate, age at maturity, age‐specific fecundity, maximum age, length‐weight and length‐egg size relationships, and other life history characteristics. We observed a strong negative relationship between maximum size and DOC concentration; for instance, fish reached masses of 150 to 260 g in low‐DOC lakes but <120 g in high‐DOC lakes. Relationships between fecundity and length, and between egg size and length, were constant across the DOC gradient. Because fish in high‐DOC lakes reached smaller sizes but had similar fecundity and egg size at a given size, their total lifetime fecundity was as much as two orders of magnitude lower than fish in low‐DOC lakes. High DOC concentrations appeared to constrain the range of bluegill life history strategies available; populations in high‐DOC lakes always had low initial growth rates and high ages at maturity, whereas populations in low‐DOC showed higher variability in these traits. This was also the case for the intrinsic rates of natural increase of these populations, which were always low at the high end of the DOC gradient. The potentially lower capacity for fish populations in high‐DOC lakes to recover from exploitation has clear implications for the sustainable management of recreational fisheries in the face of considerable spatial heterogeneity and ongoing temporal change in lake DOC concentrations.     

Ontogenetic and spatial variation in size‐selective mortality of a marine fish

Although body size can affect individual fitness, ontogenetic and spatial variation in the ecology of an organism may determine the relative advantages of size and growth. During an 8‐year field study in the Bahamas, we examined selective mortality on size and growth throughout the entire reef‐associated life phase of a common coral‐reef fish, Stegastes partitus (the bicolour damselfish). On average, faster‐growing juveniles experienced greater mortality, though as adults, larger individuals had higher survival. Comparing patterns of selection observed at four separate populations revealed that greater population density was associated with stronger selection for larger adult size. Large adults may be favoured because they are superior competitors and less susceptible to gape‐limited predators. Laboratory experiments suggested that selective mortality of fast‐growing juveniles was likely because of risk‐prone foraging behaviour. These patterns suggest that variation in ecological interactions may lead to complex patterns of lifetime selection on body size.     

Habitat-dependent and -independent plastic responses to social environment in the nine-spined stickleback (Pungitius pungitius) brain

The influence of environmental complexity on brain development has been demonstrated in a number of taxa, but the potential influence of social environment on neural architecture remains largely unexplored. We investigated experimentally the influence of social environment on the development of different brain parts in geographically and genetically isolated and ecologically divergent populations of nine-spined sticklebacks (Pungitius pungitius). Fish from two marine and two pond populations were reared in the laboratory from eggs to adulthood either individually or in groups. Group-reared pond fish developed relatively smaller brains than those reared individually, but no such difference was found in marine fish. Group-reared fish from both pond and marine populations developed larger tecta optica and smaller bulbi olfactorii than individually reared fish. The fact that the social environment effect on brain size differed between marine and pond origin fish is in agreement with the previous research, showing that pond fish pay a high developmental cost from grouping while marine fish do not. Our results demonstrate that social environment has strong effects on the development of the stickleback brain, and on the brain''s sensory neural centres in particular. The potential adaptive significance of the observed brain-size plasticity is discussed.     

Effetcs of ontogenetic scaling on resource exploitation and cohort size distributions

Variation in growth rates among individuals leading to the formation of broad size distributions is commonly observed in animal cohorts. Here we use laboratory derived size–scaling relationships to identify mechanisms driving changes in size distribution patterns within cohorts during early ontogeny. We introduced young‐of‐the‐year perch Perca fluviatilis cohorts with different variation in body size distributions in pond enclosures. We kept the exploitative competitive environment constant by adjusting the number of introduced fish such that metabolic requirements were constant between different treatments. Based on modelling results we theoretically derived relative growth rates of differently sized fish when only taken exploitative competitive interactions into account. In agreement with predictions we found that initial variation in body size was negatively correlated with subsequent changes in body size variation in the pond experiment. Corresponding results were obtained in a field study covering 13 studied young‐of‐the‐year perch cohorts in a small lake. Besides having a lower maximum growth capacity, initially large fish also suffered more from resource limitation in our experiment. The results suggest that exploitation competition is a major factor behind growth patterns in young fish cohorts, generally leading to size convergence. To explain the commonly observed pattern of size divergence in animal cohorts, including fish, we suggest that differential timing of diet shifts or mechanisms not related to exploitative interactions must be taken into account. For diet shifts to lead to size divergence we suggest that individuals with an initial size advantage need access to an exclusive prey which has a high growth potential. This, in turn, allows initially larger individuals to surf on a wave of growing prey while individuals only capable to feed on a depressed initial resource experience low growth rates.     

Geographic Variation in Age Structure and Longevity in the Nine-Spined Stickleback (Pungitius pungitius)

Variation in age and size of mature nine-spined sticklebacks (Pungitius pungitius) within and among 16 Fennoscandian populations were assessed using skeletochronology. The average age of individuals in a given population varied from 1.7 to 4.7 years. Fish from pond populations were on average older than those from lake and marine populations, and females tended to be older than males. Reproduction in marine and lake populations commenced typically at an age of two years, whereas that in ponds at an age of three years. The maximum life span of the fish varied from 3 to 7 years. Mean body size within and among populations increased with increasing age, but the habitat and population differences in body size persisted even after accounting for variation in population age (and sex) structure. Hence, the population differences in mean body size are not explainable by age differences alone. As such, much of the pronounced intraspecific variation in population age structure can be attributed to delayed maturation and extended longevity of the pond fish. The results are contrasted and discussed in the context of similar data from the three-spined stickleback (Gasterosteus aculeatus) occupying the same geographic area.     

Evolution of stickleback feeding behaviour: genetics of population divergence at different ontogenetic stages

The evolutionary significance of individual consistency in a given behaviour – called animal personality – has been subject to a lot of recent research. However, the genetic underpinnings of population divergence in mean personality have rarely been studied, especially across different ontogenetic stages. Previous work has shown that marine vs. pond populations of nine‐spined sticklebacks (Pungitius pungitius) have undergone adaptive divergence in a series of fitness‐related traits, including behaviour. One particular behavioural trait important in this system is feeding activity: giant pond sticklebacks are more active feeders than their normal sized marine conspecifics. In a common garden experiment, we raised individuals from pure and hybrid F₁‐generation crosses of a highly divergent marine – pond population pair to see if (i) feeding activity and/or its ontogenetic change was consistent between individuals, and if (ii) population divergence at different ontogenetic stages could be explained by additive genetic, nonadditive genetic or maternal effects. We found that feeding activity decreased with age, but that these changes were consistently different among both individuals and crosses. The among cross patterns were consistent with a nonadditive genetic scenario: in the early period pond sticklebacks expressed dominance for high feeding activity, while in the late period marine sticklebacks expressed dominance for low feeding activity. We conclude that nine‐spined sticklebacks exhibit different feeding personalities, and that the population divergence in feeding personality is explainable by age‐dependent expression of genetic dominance.     

Diet and a developmental time constraint alter life‐history trade‐offs in a caddis fly (Trichoptera: Limnephilidae)

Environmental factors influence variation in life histories by affecting growth, development, and reproduction. We conducted an experiment in outdoor mesocosms to examine how diet and a time constraint on juvenile development (pond‐drying) influence life‐history trade‐offs (growth, development, adult body mass) in the caddis fly Limnephilus externus (Trichoptera: Limnephilidae). We predicted that: (1) diet supplementation would accelerate larval growth and development, and enhance survival to adulthood; (2) pond‐drying would accelerate development and increase larval mortality; and (3) the relationship between adult mass and age at maturity would be negative. Diet supplementation did lead to larger adult mass under nondrying conditions, but did not significantly alter growth or development rates. Contrary to predictions, pond‐drying reduced growth rates and delayed development. The slope (positive or negative) of the female mass–age at maturity relationship depended on interactions with diet or pond‐drying, but the male mass–age relationship was negative and independent of treatment. Our results suggest that pond‐drying can have negative effects on the future fitness of individuals by increasing the risk of desiccation‐induced, pre‐reproductive mortality and decreasing adult body size at maturity. These negative effects on life history cannot be overcome with additional nutritional resources in this species. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 495–504.     

Female‐biased dimorphism in size and age at maturity is reduced at higher latitudes in lake whitefish Coregonus clupeaformis

Female‐biased sexual dimorphism in size at maturity is a common pattern observed in freshwater fishes with indeterminate growth, yet can vary in magnitude among populations for reasons that are not well understood. According to sex‐specific optimization models, female‐biased sexual size dimorphism can evolve due to sexual selection favouring earlier maturation by males, even when sexes are otherwise similar in their growth and mortality regimes. The magnitude of sexual size dimorphism is expected to depend on mortality rate. When mortality rates are low, both males and females are expected to mature at older ages and larger sizes, with size determined by the von Bertalanffy growth equation. The difference between size at maturity in males and females becomes reduced when maturing at older ages, closer to asymptotic size. This phenomenon is called von Bertalanffy buffering. The predicted relationship between the magnitude of female‐biased sexual dimorphism in age and size at maturity and mortality rate was tested in a comparative analysis of lake whitefish Coregonus clupeaformis from 26 populations across a broad latitudinal range in North America. Most C. clupeaformis populations displayed female‐biased sexual dimorphism in size and age at 50% maturity. As predicted, female‐biased sexual size dimorphism was less extreme among lower mortality, high‐latitude populations.     

Estimating growth and mortality rates from size data

Summary A method is presented for estimating rates of individual growth and population mortality utilizing average individual size at two times during a year. The model assumes a constant rate of mortality, Brody-Bertalanffy growth, a stationary age distribution, and recruitment confined to one month each year. A hypothetical example is presented to show the interrelationships of the growth and mortality constants, size at recruitment, asymptotic size and average individual size. Three examples are presented using data from the literature: Flathead sole (Hippoglossoides elassodon), a sea urchin(Echinus esculentus), and the crown-of-thorns starfish(Acanthaster planci). The method appears to be a means of obtaining reasonable approximations of growth and mortality rates for a variety of organisms.     

Quantitative trait loci for growth and body size in the nine‐spined stickleback Pungitius pungitius L.

Body size is an ecologically important trait shown to be genetically variable both within and among different animal populations as revealed by quantitative genetic studies. However, few studies have looked into underlying genetic architecture of body size variability in the wild using genetic mapping methods. With the aid of quantitative trait loci (QTL) analyses based on 226 microsatellite markers, we mapped body size and growth rate traits in the nine‐spined stickleback (Pungitius pungitius) using an F₂‐intercross (n = 283 offspring) between size‐divergent populations. In total, 17 QTL locations were detected. The proportion of phenotypic variation explained by individual body size‐related QTL ranged from 3% to 12% and those related to growth parameters and increments from 3% to 10%. Several of the detected QTL affected either early or late growth. These results provide a solid starting point for more in depth investigations of structure and function of genomic regions involved in determination of body size in this popular model of ecological and evolutionary research.