Abstract

Traditionally, the impact of evolution on the central nervous system has been studied by comparing the sizes of brain regions between species. However, more recent work has demonstrated that environmental factors, such as sensory experience, modulate brain region sizes intraspecifically, clouding the distinction between evolutionary and environmental sources of neuroanatomical variation in a sampled brain. Here, we review how teleost fish have played a central role in shaping this traditional understanding of brain structure evolution between species as well as the capacity for the environment to shape brain structure similarly within a species. By demonstrating that variation measured by brain region size varies similarly both inter- and intraspecifically, work on teleosts highlights the depth of the problem of studying brain evolution using neuroanatomy alone: even neurogenesis, the primary mechanism through which brain regions are thought to change size between species, also mediates experience-dependent changes within species. Here, we argue that teleost models also offer a solution to this overreliance on neuroanatomy in the study of brain evolution. With the advent of work on teleosts demonstrating interspecific evolutionary signatures in embryonic gene expression and the growing understanding of developmental neurogenesis as a multi-stepped process that may be differentially regulated between species, we argue that the tools are now in place to reframe how we compare brains between species. Future research can now transcend neuroanatomy to leverage the experimental utility of teleost fishes in order to gain deeper neurobiological insight to help us discern developmental signatures of evolutionary adaptation from phenotypic plasticity.

Highlights

  • The impact of evolution on the central nervous system has been studied by comparing the sizes of brain regions between species

  • With the advent of work on teleosts demonstrating interspecific evolutionary signatures in embryonic gene expression and the growing understanding of developmental neurogenesis as a multi-stepped process that may be differentially regulated between species, we argue that the tools are in place to reframe how we compare brains between species

  • What happens when neuroanatomical variation manifests between and within species? If, for example, the olfactory bulb is enlarged in one species compared to another, is this enlargement a product of evolutionary forces or a product of differences in olfactory experiences between species during neurodevelopment? Without understanding the extremes of phenotypic plasticity in neuroanatomy within a species, can we affirm that observed interspecific variation in brain structure is primarily a product of evolution and not the different environments experienced by the individuals sampled representing each species? In this perspective article, we discuss the utility of teleost fish species as animal models in addressing evolutionary and environmental sources of neuroanatomical variation

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Summary

TELEOSTS AS MODEL SPECIES IN COMPARATIVE NEUROANATOMY

Average brain size has increased during vertebrate evolution and, while much of this is due to changes in overall body size, some of this variation is due to evolutionary forces acting on brain development beyond allometric constraints (Striedter, 2005). Huber et al (1997) generated an extensive database of brain region morphology for 189 African cichlid species across three inland lakes Using comparative analysis, they reported that species evolved to engage in agile prey capture behavior exhibit larger cerebella and optic tecta, a midbrain structure and primary recipient of retinal input, compared to species evolved to feed on relatively stationary mollusks and plants. Complementary to this work, Kotrschal and Palzenberger (1992) found that bottom-feeding benthivore cyprinid species exhibit an evolutionary increase in the size of brain structures involved in processing chemosensory and olfactory input, consistent with relaxed evolutionary pressure on visual capabilities and increased importance for smell and taste while feeding along turbid lake bottoms These investigations set the stage for the concept of brain ecotypes, in which brain morphology is specialized to improve sensory processing in the modality most critical for feeding success (Sylvester et al, 2010). Research on phenotypic plasticity in teleost brains challenges this assumption, demonstrating that the environment impacts brain structure within a species

TELEOSTS AS MODEL SPECIES IN STUDYING PHENOTYPIC PLASTICITY IN NEUROANATOMY
CONCLUSION
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