Intraspecific variation in brain size and architecture : population divergence and phenotypic plasticity

Brain size and architecture exhibit great evolutionary and ontogenetic variation. Yet, studies on population variation (within a single species) in brain size and architecture, or in brain plasticity induced by ecologically relevant biotic factors have been largely overlooked. Here, I address the following questions: (i) do locally adapted populations differ in brain size and architecture, (ii) can the biotic environment induce brain plasticity, and (iii) do locally adapted populations differ in levels of brain plasticity? In the first two chapters I report large variation in both absolute and relative brain size, as well as in the relative sizes of brain parts, among divergent nine-spined stickleback (Pungitius pungitius) populations. Some traits show habitat-dependent divergence, implying natural selection being responsible for the observed patterns. Namely, marine sticklebacks have relatively larger bulbi olfactorii (chemosensory centre) and telencephala (involved in learning) than pond sticklebacks. Further, I demonstrate the importance of common garden studies in drawing firm evolutionary conclusions. In the following three chapters I show how the social environment and perceived predation risk shapes brain development. In common frog (Rana temporaria) tadpoles, I demonstrate that under the highest per capita predation risk, tadpoles develop smaller brains than in less risky situations, while high tadpole density results in enlarged tectum opticum (visual brain centre). Visual contact with conspecifics induces enlarged tecta optica in nine-spined sticklebacks, whereas when only olfactory cues from conspecifics are available, bulbus olfactorius become enlarged.Perceived predation risk results in smaller hypothalami (complex function) in sticklebacks. Further, group-living has a negative effect on relative brain size in the competition-adapted pond sticklebacks, but not in the predation-adapted marine sticklebacks. Perceived predation risk induces enlargement of bulbus olfactorius in pond sticklebacks, but not in marine sticklebacks who have larger bulbi olfactorii than pond fish regardless of predation. In sum, my studies demonstrate how applying a microevolutionary approach can help us to understand the enormous variation observed in the brains of wild animals a point-of-view which I high-light in the closing review chapter of my thesis.Aivojen koko ja rakenne muuntelee huomattavasti sekä evolutiivisesti, että yksilönkehityksen aikana. Harva tutkimus on kuitenkaan tarkastellut yhden lajin eri populaatioiden välistä erilaistumista aivojen koossa ja rakenteessa, tai sitä jos ja kuinka elinympäristö vaikuttaa aivojen koon ja rakenteen kehitykseen. Väitöskirjassani tarkastelinkin (i) onko paikallisesti sopeutuneiden populaatioiden aivojen koossa ja rakenteessa eroja, (ii) voiko ympäristö muokata aivojen kehitystä ja (iii) onko paikallisesti sopeutuneiden populaatioiden aivojen plastisuudessa eroja? Kahdessa ensimmäisessä kappaleessa tutkin kymmenpiikkipopulaatioiden (Pungitius pungitius) erilaistumista aivojen absoluuttisessa ja suhteellisessa koossa, sekä aivojen eri osien suhteellisen koon vaihtelua. Merestä peräisin olevilla kymmenpiikeillä oli suhteessa suuremmat hajukäämit (bulbi olfactorii) ja isoaivot (telencephala) kuin samassa laboratorioympäristössä kasvaneilla lampikaloilla. Tulokset antavatkin tukea tulkita populaatioiden välinen erilaistuminen aivojen koossa luonnovalinnan aiheuttamiksi paikallisiksi sopeumiksi. Työn tulokset alleviivaavat myös testiympäristön standardoinnin merkitystä evolutiivisissa tutkimuksissa. Kolmen seuraavaan kappaleen työt tarkastelevat sosiaalisen ympäristön ja saalistuksen uhan merkitystä aivojen kehityksen muokkaajina. Sammakonpoikasille (Rana temporaria) kehittyi korkean saalistusuhan alla pienemmät aivot, kun taas korkea yksilötiheys johtti aivojen visuaalisen keskuksen (tectum opticumin) kehityksen korostumiseen. Kymmenpiikeillä näköyhteys lajitovereihin kasvatti visuaalisen keskuksen kokoa, kun taas hajuyhteys lajitovereihin kasvatti hajukäämien kokoa. Saalistuksen uhka pienensi myös väliaivojen pohjaosaa (hypothalamusta). Myös parvessa eläminen vaikutti negatiivisesti aivojen suhteelliseen koon kehitykseen kilpailuun sopeutuneilla lampikaloilla, mutta ei saalistukseen sopeutuneilla merikaloilla. Saalistuksen uhka edisti lampikymmenpiikkien hajukäämien kehitystä, mutta ei merikymmenpiikkien joilla on lampikaloja suuremmat hajukäämit saalistuksen uhasta riippumatta. Yhteenvetona voidaan todeta, että tutkimukseni osoittavat kuinka mikroevolutiivinen lähestymistapa antaa meille mahdollisuuden ymmärtää niitä evolutiivisia valintapaineita jotka ovat johtaneet aivojen koon ja rakenteen valtavaan monimuotoisuuteen. Tätä näkökulmaa korostan väitöskirjani viimeisessä kappaleessa, joka on kattava katsaus töihin, joissa on tarkasteltu aivojen erilaistumista eri populaatioiden välillä

Quantitative genetic analysis of brain size variation in sticklebacks: support for the mosaic model of brain evolution

The mosaic model of brain evolution postulates that different brain regions are relatively free to evolve independently from each other. Such independent evolution is possible only if genetic correlations among the different brain regions are less than unity. We estimated heritabilities, evolvabilities and genetic correlations of relative size of the brain, and its different regions in the three-spined stickleback (Gasterosteus aculeatus). We found that heritabilities were low (average h2 = 0.24), suggesting a large plastic component to brain architecture. However, evolvabilities of different brain parts were moderate, suggesting the presence of additive genetic variance to sustain a response to selection in the long term. Genetic correlations among different brain regions were low (average rG = 0.40) and significantly less than unity. These results, along with those from analyses of phenotypic and genetic integration, indicate a high degree of independence between different brain regions, suggesting that responses to selection are unlikely to be severely constrained by genetic and phenotypic correlations. Hence, the results give strong support for the mosaic model of brain evolution. However, the genetic correlation between brain and body size was high (rG = 0.89), suggesting a constraint for independent evolution of brain and body size in sticklebacks

Experimental evidence for sex-specific plasticity in adult brain

Abstract Background Plasticity in brain size and the size of different brain regions during early ontogeny is known from many vertebrate taxa, but less is known about plasticity in the brains of adults. In contrast to mammals and birds, most parts of a fish’s brain continue to undergo neurogenesis throughout adulthood, making lifelong plasticity in brain size possible. We tested whether maturing adult three-spined sticklebacks (Gasterosteus aculeatus) reared in a stimulus-poor environment exhibited brain plasticity in response to environmental enrichment, and whether these responses were sex-specific, thus altering the degree of sexual size dimorphism in the brain. Results Relative sizes of total brain and bulbus olfactorius showed sex-specific responses to treatment: males developed larger brains but smaller bulbi olfactorii than females in the enriched treatment. Hence, the degree of sexual size dimorphism (SSD) in relative brain size and the relative size of the bulbus olfactorius was found to be environment-dependent. Furthermore, the enriched treatment induced development of smaller tecta optica in both sexes. Conclusions These results demonstrate that adult fish can alter the size of their brain (or brain regions) in response to environmental stimuli, and these responses can be sex-specific. Hence, the degree of SSD in brain size can be environment-dependent, and our results hint at the possibility of a large plastic component to SSD in stickleback brains. Apart from contributing to our understanding of the processes shaping and explaining variation in brain size and the size of different brain regions in the wild, the results show that provision of structural complexity in captive environments can influence brain development. Assuming that the observed plasticity influences fish behaviour, these findings may also have relevance for fish stocking, both for economical and conservational purposes

Population variation in brain size of nine-spined sticklebacks (Pungitius pungitius) - local adaptation or environmentally induced variation?

Abstract Background Most 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. Results Brain 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. Conclusion Our 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.</p

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

Evidence for sex-specific selection in brain: a case study of the nine-spined stickleback

Theory predicts that the sex making greater investments into reproductive behaviours demands higher cognitive ability, and as a consequence, larger brains or brain parts. Further, the resulting sexual dimorphism can differ between populations adapted to different environments, or among individuals developing under different environmental conditions. In the nine-spine stickleback (Pungitius pungitius), males perform nest building, courtship, territory defence and parental care, whereas females perform mate choice and produce eggs. Also, predation-adapted marine and competition-adapted pond populations have diverged in a series of ecologically relevant traits, including the level of phenotypic plasticity. Here, we studied sexual dimorphism in brain size and architecture in nine-spined stickleback from marine and pond populations reared in a factorial experiment with predation and food treatments in a common garden experiment. Males had relatively larger brains, larger telencephala, cerebella and hypothalami (6–16% divergence) than females, irrespective of habitat. Females tended to have larger bulbi olfactorii than males (13%) in the high food treatment, whereas no such difference was found in the low food treatment. The strong sexual dimorphism in brain architecture implies that the different reproductive allocation strategies (behaviour vs. egg production) select for different investments into the costly brains between males and females. The lack of habitat dependence in brain sexual dimorphism suggests that the sex-specific selection forces on brains differ only negligibly between habitats. Although significance of the observed sex-specific brain plasticity in the size of bulbus olfactorius remains unclear, it demonstrates the potential for sex-specific neural plasticity

Evidence for sex-specific selection in brain: a case study of the nine-spined stickleback.

Theory predicts that the sex making greater investments into reproductive behaviours demands higher cognitive ability, and as a consequence, larger brains or brain parts. Further, the resulting sexual dimorphism can differ between populations adapted to different environments, or among individuals developing under different environmental conditions. In the nine-spine stickleback (Pungitius pungitius), males perform nest building, courtship, territory defence and parental care, whereas females perform mate choice and produce eggs. Also, predation-adapted marine and competition-adapted pond populations have diverged in a series of ecologically relevant traits, including the level of phenotypic plasticity. Here, we studied sexual dimorphism in brain size and architecture in nine-spined stickleback from marine and pond populations reared in a factorial experiment with predation and food treatments in a common garden experiment. Males had relatively larger brains, larger telencephala, cerebella and hypothalami (6–16% divergence) than females, irrespective of habitat. Females tended to have larger bulbi olfactorii than males (13%) in the high food treatment, whereas no such difference was found in the low food treatment. The strong sexual dimorphism in brain architecture implies that the different reproductive allocation strategies (behaviour vs. egg production) select for different investments into the costly brains between males and females. The lack of habitat dependence in brain sexual dimorphism suggests that the sex-specific selection forces on brains differ only negligibly between habitats. Although significance of the observed sex-specific brain plasticity in the size of bulbus olfactorius remains unclear, it demonstrates the potential for sex-specific neural plasticity

Data from: Evidence for sex-specific selection in brain: a case study of the nine-spined stickleback

Theory predicts that the sex making greater investments into reproductive behaviours demands higher cognitive ability, and as a consequence, larger brains or brain parts. Further, the resulting sexual dimorphism can differ between populations adapted to different environments, or among individuals developing under different environmental conditions. In the nine-spine stickleback (Pungitius pungitius), males perform nest building, courtship, territory defence and parental care, whereas females perform mate choice and produce eggs. Also, predation-adapted marine and competition-adapted pond populations have diverged in a series of ecologically relevant traits, including the level of phenotypic plasticity. Here, we studied sexual dimorphism in brain size and architecture in nine-spined stickleback from marine and pond populations reared in a factorial experiment with predation and food treatments in a common garden experiment. Males had relatively larger brains, larger telencephala, cerebella and hypothalami (6–16% divergence) than females, irrespective of habitat. Females tended to have larger bulbi olfactorii than males (13%) in the high food treatment, whereas no such difference was found in the low food treatment. The strong sexual dimorphism in brain architecture implies that the different reproductive allocation strategies (behaviour vs. egg production) select for different investments into the costly brains between males and females. The lack of habitat dependence in brain sexual dimorphism suggests that the sex-specific selection forces on brains differ only negligibly between habitats. Although significance of the observed sex-specific brain plasticity in the size of bulbus olfactorius remains unclear, it demonstrates the potential for sex-specific neural plasticity

metamorph brains

Experimental treatments included low and high larval density, crossed with the presence and absence of a caged predator. 100 tadpoles from each of the 12 clutches were pooled into a bucket and allocated to each tank (high density = 50 tadpoles/tank; low density = 10 tadpoles/tank). In tanks with the predator treatments, one dragonfly larva (Aeshna sp.) was placed in a cylindrical cage (diameter 8 cm; height 21 cm) made of transparent plastic film with a double net bottom (mesh size 1.5 mm) and hung 6 cm over the tank bottom. This allowed tadpoles to receive both visual and chemical cues from the predator, while the predator was unable to actually prey on tadpoles. In the no-predator treatment, the cage was left empty. During the experiment, tadpoles relied on the initial resources provided (leaves, rabbit pellets), as well as subsequent algal growth. Each treatment combination was replicated eight times, resulting in a total of 32 experimental units. 143 metamorphs (four to five per tank) were used for analyses. Formalin fixed metamorphs were weighed with a digital balance. After dissection, dorsal and right lateral views of brains were photographed with a digital camera connected to a dissecting microscope. We could only measure two dimensions for each brain part (length and width of telencephalon, diencephalon and optic tectum, and height and width of medulla oblongata) because some of the borders of the brain parts could not be identified accurately. Measurements were taken from digital photographs using tpsDig 1.37 software, and were defined as the greatest distance enclosed by the given structure in the given direction. All brains were photographed and measured three times. Repeatability of different brain measurements was high (R = 0.71 – 0.96 [mean = 0.86])