Evo-Devo and Brain Scaling: Candidate Developmental Mechanisms for Variation and Constancy in Vertebrate Brain Evolution

Charvet, Christine J.; Striedter, Georg F.; Finlay, Barbara L.

doi:10.1159/000329851

Cited by 81 publications

(64 citation statements)

References 180 publications

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“…Variation in the timing of neurogenesis, cell-cycle rates and patterning of progenitor pools suggest these processes can, at least in part, evolve independently [104], offering alternative routes through which selection can act. These three routes to the diversification of brain structure may take effect at different stages of development.…”

Section: (E) Developmental Models Of Mosaic Evolutionmentioning

confidence: 99%

Brain evolution and development: adaptation, allometry and constraint

2016

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Phenotypic traits are products of two processes: evolution and development. But how do these processes combine to produce integrated phenotypes? Comparative studies identify consistent patterns of covariation, or allometries, between brain and body size, and between brain components, indicating the presence of significant constraints limiting independent evolution of separate parts. These constraints are poorly understood, but in principle could be either developmental or functional. The developmental constraints hypothesis suggests that individual components (brain and body size, or individual brain components) tend to evolve together because natural selection operates on relatively simple developmental mechanisms that affect the growth of all parts in a concerted manner. The functional constraints hypothesis suggests that correlated change reflects the action of selection on distributed functional systems connecting the different sub-components, predicting more complex patterns of mosaic change at the level of the functional systems and more complex genetic and developmental mechanisms. These hypotheses are not mutually exclusive but make different predictions. We review recent genetic and neurodevelopmental evidence, concluding that functional rather than developmental constraints are the main cause of the observed patterns. How brains evolve: the importance of scaling relationshipsThe components of any adaptive complex by definition undergo coordinated evolution. Brains, bodies and individual brain components therefore exhibit distinctive patterns of correlated evolution. But what do these patterns tell us about the roles of adaptation and constraint in shaping phenotypes? In particular, how and to what extent do constraints imposed by shared developmental programmes dictate allometric relationships between components, limiting their response to selection? These questions have shaped two key debates central to how we view brain evolution: the functional relevance of brain size and the adaptive potential of brain structure [1][2][3]. These debates hinge on whether observed patterns of scaling relationships, between brain and body size or different brain components, are the product of selection to maintain functional correspondence or constraints imposed by shared developmental programmes. Crucially, however, a sound understanding of the significance of scaling relationships in brain evolution has been limited by a lack of data on the genetic and developmental mechanisms that regulate brain size and structure. Here we discuss how recent discoveries about the genetic control of neural development shed new light on the issue.(a) Brain: body coevolution and the importance of size

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Section: (E) Developmental Models Of Mosaic Evolutionmentioning

confidence: 99%

Brain evolution and development: adaptation, allometry and constraint

2016

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“…In mammals, the volumes of the major brain subdivisions appear to be evolving primarily in concert [Finlay and Darlington, 1995;Whiting and Barton, 2003;Striedter, 2005] whereas in birds, the major brain subdivisions seem to be evolving as a mosaic [Boire and Baron, 1994;Iwaniuk et al, 2004]. However, all groups show evidence of both processes, since there is also evidence for mosaic brain evolution in mammals [Barton and Harvey, 2000;Brown, 2001;Dobson and Sherwood, 2011;Hager et al, 2012] and concerted brain evolution in birds [Charvet et al, 2011;Gutiér-rez-Ibáñez et al, 2014]. This dichotomy also exists between the major clades of fishes, with cartilaginous fishes primarily showing a concerted pattern of brain evolution [Yopak et al, 2010] whereas bony fishes seem to primarily exhibit a mosaic pattern [Kotrschal et al, 1998;Gonzalez-Voyer et al, 2009].…”

Section: Introductionmentioning

confidence: 99%

Evidence for Concerted and Mosaic Brain Evolution in Dragon Lizards

et al. 2017

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is unclear. Here, we examined the volumes of the 6 major neural subdivisions across 14 species of the agamid lizard genus Ctenophorus (dragons). These species have diverged multiple times in behaviour, ecology, and body morphology, affording a unique opportunity to test neuroevolutionary models across species. We assigned each species to an ecomorph based on habitat use and refuge type, then used MRI to measure total and regional brain volume. We found evidence for both mosaic and concerted brain evolution in dragons: concerted brain evolution with respect to body size, and mosaic brain evolution with respect to ecomorph. Specifically, all brain subdivisions increase in volume relative to body size, yet the tectum and rhombencephalon also show opposite patterns of evolution with respect to ecomorph. Therefore, we find that both models of evolution are occurring simultaneously in the same structures in dragons, but are only detectable when examining particular drivers of selection. We show that the answer to the question of whether concerted or mosaic brain evolution is detected in a system can depend more on the type of selection measured than on the clade of animals studied. AbstractThe brain plays a critical role in a wide variety of functions including behaviour, perception, motor control, and homeostatic maintenance. Each function can undergo different selective pressures over the course of evolution, and as selection acts on the outputs of brain function, it necessarily alters the structure of the brain. Two models have been proposed to explain the evolutionary patterns observed in brain morphology. The concerted brain evolution model posits that the brain evolves as a single unit and the evolution of different brain regions are coordinated. The mosaic brain evolution model posits that brain regions evolve independently of each other. It is now understood that both models are responsible for driving changes in brain morphology; however, which factors favour concerted or mosaic brain evolution

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“…Recent work in evolutionary developmental neurobiology has shown that these evolutionary increases in brain region volumes are often caused by delays in cell cycle exit of neuronal precursors (5,6). Among birds, for example, parrots and songbirds exhibit delayed telencephalic neurogenesis relative to chicken-like birds (7)(8)(9).…”

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Expansion, folding, and abnormal lamination of the chick optic tectum after intraventricular injections of FGF2

McGowan

Alaama

Freise

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Comparative research has shown that evolutionary increases in brain region volumes often involve delays in neurogenesis. However, little is known about the influence of such changes on subsequent development. To get at this question, we injected FGF2-which delays cell cycle exit in mammalian neocortex-into the cerebral ventricles of chicks at embryonic day (ED) 4. This manipulation alters the development of the optic tectum dramatically. By ED7, the tectum of FGF2-treated birds is abnormally thin and has a reduced postmitotic layer, consistent with a delay in neurogenesis. FGF2 treatment also increases tectal volume and ventricular surface area, disturbs tectal lamination, and creates small discontinuities in the pia mater overlying the tectum. On ED12, the tectum is still larger in FGF2-treated embryos than in controls. However, lateral portions of the FGF2-treated tectum now exhibit volcano-like laminar disturbances that coincide with holes in the pia, and the caudomedial tectum exhibits prominent folds. To explain these observations, we propose that the tangential expansion of the ventricular surface in FGF2-treated tecta outpaces the expansion of the pial surface, creating abnormal mechanical stresses. Two alternative means of alleviating these stresses are tectal foliation and the formation of pial holes. The latter probably alter signaling gradients required for normal cell migration and may generate abnormal patterns of cerebrospinal fluid flow; both abnormalities would generate disturbances in tectal lamination. Overall, our findings suggest that evolutionary expansion of sheet-like, laminated brain regions requires a concomitant expansion of the pia mater.brain evolution | evolutionary developmental biology | proliferation | meninges | cortical folding E volutionary increases in brain region volumes are common (1).For example, the neocortex is disproportionately enlarged in primates relative to other mammals, and the telencephalon is disproportionately enlarged in parrots and songbirds relative to other birds (1-4). Recent work in evolutionary developmental neurobiology has shown that these evolutionary increases in brain region volumes are often caused by delays in cell cycle exit of neuronal precursors (5, 6). Among birds, for example, parrots and songbirds exhibit delayed telencephalic neurogenesis relative to chicken-like birds (7-9). Among mammals, cell cycle exit in the neocortex is similarly delayed in primates, which have a disproportionately enlarged neocortex (5, 10-12).Unfortunately, the downstream effects of delayed cell cycle exit on subsequent developmental processes and adult morphology remain poorly understood. One way to fill this gap in our knowledge is to experimentally recreate the key species differences in the laboratory by means of carefully selected developmental manipulations. A good example of this phenocopy approach was the creation of transgenic mice with a constitutively active form of β-catenin that prolongs proliferation, increases neocortical volume, and generates cortica...

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Evo-Devo and Brain Scaling: Candidate Developmental Mechanisms for Variation and Constancy in Vertebrate Brain Evolution

Cited by 81 publications

References 180 publications

Brain evolution and development: adaptation, allometry and constraint

Brain evolution and development: adaptation, allometry and constraint

Evidence for Concerted and Mosaic Brain Evolution in Dragon Lizards

Expansion, folding, and abnormal lamination of the chick optic tectum after intraventricular injections of FGF2

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