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 (ninespined 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.

BackgroundMost evolutionary studies on the size of brains and different parts of the brain have relied on interspecific comparisons, and have uncovered correlations between brain architecture and various ecological, behavioural and life-history traits. Yet, similar intraspecific studies are rare, despite the fact that they could better determine how selection and phenotypic plasticity influence brain architecture. We investigated the variation in brain size and structure in wild-caught nine-spined sticklebacks (Pungitius pungitius) from eight populations, representing marine, lake, and pond habitats, and compared them to data from a previous common garden study from a smaller number of populations.ResultsBrain size scaled hypo-allometrically with body size, irrespective of population origin, with a common slope of 0.5. Both absolute and relative brain size, as well as relative telencephalon, optic tectum and cerebellum size, differed significantly among the populations. Further, absolute and relative brain sizes were larger in pond than in marine populations, while the telencephalon tended to be larger in marine than in pond populations. These findings are partly incongruent with previous common garden results. A direct comparison between wild and common garden fish from the same populations revealed a habitat-specific effect: pond fish had relatively smaller brains in a controlled environment than in the wild, while marine fish were similar. All brain parts were smaller in the laboratory than in the wild, irrespective of population origin.ConclusionOur results indicate that variation among populations is large, both in terms of brain size and in the size of separate brain parts in wild nine-spined sticklebacks. However, the incongruence between the wild and common garden patterns suggests that much of the population variation found in the wild may be attributable to environmentally induced phenotypic plasticity. Given that the brain is among the most plastic organs in general, the results emphasize the view that common garden data are required to draw firm evolutionary conclusions from patterns of brain size variability in the wild.

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.

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.

The brain is a trait of central importance for organismal performance and fitness. To date, evolutionary studies of brain size variation have mainly utilized comparative methods applied at the level of species or higher taxa. However, these studies suffer from the difficulty of separating causality from correlation. In the other extreme, studies of brain plasticity have focused mainly on within-population patterns. Between these extremes lie interpopulational studies, focusing on brain size variation among populations of the same species that occupy different habitats or selective regimes. These studies form a rapidly growing field of investigations which can help us to understand brain evolution by providing a test bed for ideas born out of interspecific studies, as well as aid in uncovering the relative importance of genetic and environmental factors shaping variation in brain size and architecture. Aside from providing the first in depth review of published intraspecific studies of brain size variation, we discuss the prospects embedded with interpopulational studies of brain size variation. In particular, the following topics are identified as deserving further attention: (i) studies focusing on disentangling the contributions of genes, environment, and their interactions on brain variation within and among populations, (ii) studies applying quantitative genetic tools to evaluate the relative importance of genetic and environmental factors on brain features at different ontogenetic stages, (iii) apart from utilizing simple gross estimates of brain size, future studies could benefit from use of neuroanatomical, neurohistological, and/or molecular methods in characterizing variation in brain size and architecture.

The proximate and ultimate explanations for behavioural syndromes (correlated behaviours – a population trait) are poorly understood, and the evolution of behavioural types (configuration of behaviours – an individual trait) has been rarely studied. We investigated population divergence in behavioural syndromes and types using individually reared, completely predator‐ or conspecific‐naïve adult nine‐spined sticklebacks (Pungitius pungitius) from two marine and two predatory fish free, isolated pond populations. We found little evidence for the existence of behavioural syndromes, but population divergence in behavioural types was profound: individuals from ponds were quicker in feeding, bolder and more aggressive than individuals from marine environments. Our data reject the hypothesis that behavioural syndromes exist as a result of genetic correlations between behavioural traits, and support the contention that different behavioural types can be predominant in populations differing in predation pressure, most probably as a result of repeated independent evolution of separate behavioural traits.

Summary1. Allometric scaling of sexual size dimorphism (SSD) with body size is a commonplace occurrence in intraspecific or interspecific comparisons. Typically, SSD increases with body size when males, and decreases when females are the larger sex -a pattern known as Rensch's rule. Intraspecific studies of Rensch's rule in vertebrates are extremely scarce. 2. In an allometric SSD-body size relationship, the sex with the larger body size variation is the driver of size divergence whereas the other sex is following it owing to correlational selection. Hence, one can test which sex is responsible for the observed body size divergence within this framework. 3. Nine-spined stickleback (Pungitius pungitius) provides an excellent model to study intraspecific variation in SSD owing to the large interpopulation variation in mean body size. Using data on body size variation in 11 nine-spined stickleback populations covering the full known size range of the species, we investigated: (i) whether variation in SSD scales allometrically with mean body size across the populations; (ii) which sex is driving the allometric relationship and (iii) whether the observed pattern is likely to have a genetic component. In addition, we analysed the size dependency of female reproductive output. 4. We found strong support for an inverse of Rensch's rule: level of female-biased SSD increased with increasing mean size while females were the more variable sex. Results from a common garden experiment supported the pattern found in the wild. Females from giant populations had 2-3 times larger reproductive output than normal-sized females. 5. The fact that females were the more variable sex indicates that the evolution of gigantism in nine-spined sticklebacks is driven by females, and the 2-3 times larger reproductive output per clutch of giant vs. normal-sized females suggests fecundity selection to have an important role in it. Our results oppose the commonly held view that males drive the evolution of SSD as a result of sexual selection favouring larger males.

Although the brain is known to be a very plastic organ, the effects of common ecological interactions like predation or competition on brain development have remained largely unexplored. We reared nine-spined sticklebacks (Pungitius pungitius) from two coastal marine (predation-adapted) and two isolated pond (competition-adapted) populations in a factorial experiment, manipulating perceived predatory risk and food supply to see (i) if the treatments affected brain development and (ii) if there was population differentiation in the response to treatments. We detected differences in plasticity of the bulbus olfactorius (chemosensory centre) between habitats: marine fish were not plastic, whereas pond fish had larger bulbi olfactorii in the presence of perceived predation. Marine fish had larger bulbus olfactorius overall. Irrespective of population origin, the hypothalamus was smaller in the presence of perceived predatory risk. Our results demonstrate that perceived predation risk can influence brain development, and that the effect of an environmental factor on brain development may depend on the evolutionary history of a given population in respect to this environmental factor.