Diversity of intraspecific patterns of brain region size covariation in fish.

Traits often do not evolve in isolation or vary independently of other traits. Instead, they can be affected by covariation, both within and across species. However, the importance of within species trait covariation and, critically, the degree to which it varies between species has yet to be thoroughly studied. Brain morphology is a trait of great ecological and behavioral importance, with regions that are hypothesized to vary in size based on behavioral and cognitive demands. Sizes of brain regions have also been shown to covary with each other across various taxa. Here we test the degree to which covariation in brain region sizes within species has been conserved across ten teleost fish species. These ten species span five orders, allowing us to examine how phylogenetic proximity influences similarities in intraspecific trait covariation. Our results showed a trend that similar patterns of brain region size covariation occur in more closely related species. Interestingly, there were certain brain region pairs that showed similar levels of covariation across all species regardless of phylogenetic distance, such as the telencephalon and optic tectum, while others, such as the olfactory bulb and the hypothalamus, varied more independently. Ultimately, the patterns of brain region covariation shown here suggest that evolutionary mechanisms or constraints can act on specific brain regions independently, and that these constraints can change over evolutionary time.

Evolutionary divergence of plasticity in brain morphology between ecologically divergent habitats of Trinidadian guppies.

Phenotypic plasticity is critical for organismal performance and can evolve in response to natural selection. Brain morphology is often developmentally plastic, affecting animal performance in a variety of contexts. However, the degree to which the plasticity of brain morphology evolves has rarely been explored. Here, we use Trinidadian guppies (Poecilia reticulata), which are known for their repeated adaptation to high-predation (HP) and low-predation (LP) environments, to examine the evolution and plasticity of brain morphology. We exposed second-generation offspring of individuals from HP and LP sites to 2 different treatments: predation cues and conspecific social environment. Results show that LP guppies had greater plasticity in brain morphology compared to their ancestral HP population, suggesting that plasticity can evolve in response to environmentally divergent habitats. We also show sexual dimorphism in the plasticity of brain morphology, highlighting the importance of considering sex-specific variation in adaptive diversification. Overall, these results may suggest the evolution of brain morphology plasticity as an important mechanism that allows for ecological diversification and adaptation to divergent habitats.

Embracing the diversity in diverse warning signals.

Positive frequency-dependent selection should theoretically lead to monomorphic warning coloration. Instead, numerous examples of polymorphic warning signals exist. Biases - for example, in human perception - hinder our appreciation and research of understanding warning signal diversity. We propose strategies to counter such biases and objectively move our field forward.

Evolutionary divergence of developmental plasticity and learning of mating tactics in Trinidadian guppies.

Behavioural plasticity is a major driver in the early stages of adaptation, but its effects in mediating evolution remain elusive because behavioural plasticity itself can evolve. In this study, we investigated how male Trinidadian guppies (Poecilia reticulata) adapted to different predation regimes diverged in behavioural plasticity of their mating tactic. We reared F2 juveniles of high- or low-predation population origins with different combinations of social and predator cues and assayed their mating behaviour upon sexual maturity. High-predation males learned their mating tactic from conspecific adults as juveniles, while low-predation males did not. High-predation males increased courtship when exposed to chemical predator cues during development; low-predation males decreased courtship in response to immediate chemical predator cues, but only when they were not exposed to such cues during development. Behavioural changes induced by predator cues were associated with developmental plasticity in brain morphology, but changes acquired through social learning were not. We thus show that guppy populations diverged in their response to social and ecological cues during development, and correlational evidence suggests that different cues can shape the same behaviour via different neural mechanisms. Our study demonstrates that behavioural plasticity, both environmentally induced and socially learnt, evolves rapidly and shapes adaptation when organisms colonize ecologically divergent habitats.

La plasticidad conductual es un factor importante en las primeras fases de adaptación, pero se conocen poco sus efectos sobre la evolución porque la plasticidad conductual en sí puede evolucionar. En este estudio, investigamos cómo los machos del guppy de Trinidad (Poecilia reticulata) adaptados a regímenes de depredación diferentes, han divergido en la plasticidad de su táctica de apareamiento. Criamos juveniles provenientes de poblaciones de alta y baja depredación hasta segunda generación (F2) bajo diferentes combinaciones de señales sociales y de depredación, y evaluamos su comportamiento de apareamiento al llegar a la madurez sexual. Los machos de alta depredación aprendieron su táctica de apareamiento de sus conespecíficos adultos, mientras que los machos de baja depredación no. Los machos de alta depredación aumentaron su cortejo al ser expuestos a señales de depredadores durante su desarrollo; mientras que los machos de baja depredación redujeron su cortejo en respuesta a señales inmediatas de depredadores, pero tan solo cuando no fueron expuestos a tales señales durante el desarrollo. Los cambios conductuales observados inducidos por las señales de depredación están asociados con una plasticidad en el desarrollo de la morfología cerebral, pero los cambios adquiridos por aprendizaje social no. En conclusión, demostramos que las poblaciones de guppy han divergido en su respuesta a señales sociales y ecológicas durante su desarrollo, y mostramos evidencia correlativa que sugiere que diferentes tipos de señales pueden influenciar el mismo comportamiento via mecanismos neuronales diferentes. Nuestro estudio muestra que la plasticidad conductual, tanto inducida por el medio ambiente combo aprendida socialmente, evoluciona rápidamente e influencia la adaptación durante la colonización de hábitats ecológicamente divergentes.

Integrating neuroplasticity and evolution.

Neuroplasticity and evolutionary biology have been prominent fields of study for well over a century. However, they have advanced largely independently, without consideration of the benefits of integration. We propose a new framework by which researchers can begin to examine the evolutionary causes and consequences of neuroplasticity. Neuroplasticity can be defined as changes to the structure, function or connections of the nervous system in response to individual experience. Evolution can alter levels of neuroplasticity if there is variation in neuroplasticity traits within and between populations. Neuroplasticity may be favored or disfavored by natural selection depending on the variability of the environment and the costs of neuroplasticity. Additionally, neuroplasticity may affect rates of genetic evolution in many ways: for example, decreasing rates of evolution by buffering against selection or increasing them via the Baldwin effect, by increasing genetic variation or by incorporating evolved peripheral changes to the nervous system. These mechanisms can be tested using comparative and experimental approaches and by examining patterns and consequences of variation in neuroplasticity among species, populations and individuals.

Evolutionary divergence in phenotypic plasticity shapes brain size variation between coexisting sunfish ecotypes.

Mechanisms that generate brain size variation and the consequences of such variation on ecological performance are poorly understood in most natural animal populations. We use a reciprocal-transplant common garden experiment and foraging performance trials to test for brain size plasticity and the functional consequences of brain size variation in Pumpkinseed sunfish (Lepomis gibbosus) ecotypes that have diverged between nearshore littoral and offshore pelagic lake habitats. Different age-classes of wild-caught juveniles from both habitats were exposed for 6 months to treatments that mimicked littoral and pelagic foraging. Plastic responses in oral jaw size suggested that treatments mimicked natural habitat-specific foraging conditions. Plastic brain size responses to foraging manipulations differed between ecotypes, as only pelagic sourced fish showed brain size plasticity. Only pelagic juveniles under 1 year-old expressed this plastic response, suggesting that plastic brain size responses decline with age and so may be irreversible. Finally, larger brain size was associated with enhanced foraging performance on live benthic but not pelagic prey, providing the first experimental evidence of a relationship between brain size and prey-specific foraging performance in fishes. The recent post-glacial origin of these ecotypes suggests that brain size plasticity can rapidly evolve and diverge in fish under contrasting ecological conditions.

Interspecific and intraspecific comparisons reveal the importance of evolutionary context in sunfish brain form divergence.

Habitats can select for specialized phenotypic characteristics in animals. However, the consistency of evolutionary responses to particular environmental conditions remains difficult to predict. One trait of great ecological importance is brain form, which is expected to vary between habitats that differ in their cognitive requirements. Here, we compared divergence in brain form and oral jaw size across a common littoral-pelagic ecological axis in two sunfishes at both the intraspecific and interspecific levels. Brain form differed between habitats at every level of comparison; however, divergence was inconsistent, despite consistent differences in oral jaw size. Pumpkinseed and bluegill species differed in cerebellum, optic tectum and olfactory bulb size. These differences are consistent with a historical ecological divergence because they did not manifest between littoral and pelagic ecotypes within either species, suggesting constraints on changes to these regions over short evolutionary time scales. There were also differences in brain form between conspecific ecotypes, but they were inconsistent between species. Littoral pumpkinseed had larger brains than their pelagic counterpart, and littoral bluegill had smaller telencephalons than their pelagic counterpart. Inconsistent brain form divergence between conspecific ecotypes of pumpkinseed and bluegill sharing a common littoral-pelagic habitat axis suggests that contemporary ecological conditions and historic evolutionary context interact to influence evolutionary changes in brain form in fishes.

Isolating the effects of ontogenetic niche shift on brain size development using pumpkinseed sunfish ecotypes.

A functional relationship between relative brain size and cognitive performance has been hypothesized. However, the influence of ontogenetic niche shifts on cognitive performance is not well understood. Increases in body size can affect niche use but distinguishing nonecologically relevant brain development from effects associated with ecology is difficult. If survival is enhanced by functional changes in ecocognitive performance over ontogeny, then brain size development should track ontogenetic shifts in ecology. We control for nonecologically relevant brain size development by comparing brain growth between two ecotypes of Pumpkinseed sunfish whose ecologies diverge over ontogeny from a shared juvenile niche. Brain size differs between ecotypes from their birth year onwards even though their foraging ecology appears to diverge at age 3. This finding suggests that the eco-cognitive requirements of adult niches shape early life brain growth more than the requirements of juvenile ecology.

Intraspecific brain size variation between coexisting sunfish ecotypes.

Variation in spatial complexity and foraging requirements between habitats can impose different cognitive demands on animals that may influence brain size. However, the relationship between ecologically related cognitive performance and brain size is not well established. We test whether variation in relative brain size and brain region size is associated with habitat use within a population of pumpkinseed sunfish composed of different ecotypes that inhabit either the structurally complex shoreline littoral habitat or simpler open-water pelagic habitat. Sunfish using the littoral habitat have on average 8.3% larger brains than those using the pelagic habitat. We found little difference in the proportional sizes of five brain regions between ecotypes. The results suggest that cognitive demands on sunfish may be reduced in the pelagic habitat given no habitat-specific differences in body condition. They also suggest that either a short divergence time or physiological processes may constrain changes to concerted, global modifications of brain size between sunfish ecotypes.