An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution

Abstract Background Vertebrate brain structure is characterised not only by relative consistency in scaling between components, but also by many examples of divergence from these general trends.. Alternative hypotheses explain these patterns by emphasising either ‘external’ processes, such as coordi...

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Main Authors: Shahar Avin, Adrian Currie, Stephen H. Montgomery
Format: Article
Language:English
Published: BMC 2021-05-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-021-01024-1
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author Shahar Avin
Adrian Currie
Stephen H. Montgomery
author_facet Shahar Avin
Adrian Currie
Stephen H. Montgomery
author_sort Shahar Avin
collection DOAJ
description Abstract Background Vertebrate brain structure is characterised not only by relative consistency in scaling between components, but also by many examples of divergence from these general trends.. Alternative hypotheses explain these patterns by emphasising either ‘external’ processes, such as coordinated or divergent selection, or ‘internal’ processes, like developmental coupling among brain regions. Although these hypotheses are not mutually exclusive, there is little agreement over their relative importance across time or how that importance may vary across evolutionary contexts. Results We introduce an agent-based model to simulate brain evolution in a ‘bare-bones’ system and examine dependencies between variables shaping brain evolution. We show that ‘concerted’ patterns of brain evolution do not, in themselves, provide evidence for developmental coupling, despite these terms often being treated as synonymous in the literature. Instead, concerted evolution can reflect either functional or developmental integration. Our model further allows us to clarify conditions under which such developmental coupling, or uncoupling, is potentially adaptive, revealing support for the maintenance of both mechanisms in neural evolution. Critically, we illustrate how the probability of deviation from concerted evolution depends on the cost/benefit ratio of neural tissue, which increases when overall brain size is itself under constraint. Conclusions We conclude that both developmentally coupled and uncoupled brain architectures can provide adaptive mechanisms, depending on the distribution of selection across brain structures, life history and costs of neural tissue. However, when constraints also act on overall brain size, heterogeneity in selection across brain structures will favour region specific, or mosaic, evolution. Regardless, the respective advantages of developmentally coupled and uncoupled brain architectures mean that both may persist in fluctuating environments. This implies that developmental coupling is unlikely to be a persistent constraint, but could evolve as an adaptive outcome to selection to maintain functional integration.
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spelling doaj.art-ac84d97c87194458ad89748be3ac2d1f2022-12-21T21:28:14ZengBMCBMC Biology1741-70072021-05-0119111810.1186/s12915-021-01024-1An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolutionShahar Avin0Adrian Currie1Stephen H. Montgomery2Centre for the Study of Existential Risk, University of CambridgeDepartment of Sociology, Philosophy and Anthropology, University of ExeterSchool of Biological Sciences, University of BristolAbstract Background Vertebrate brain structure is characterised not only by relative consistency in scaling between components, but also by many examples of divergence from these general trends.. Alternative hypotheses explain these patterns by emphasising either ‘external’ processes, such as coordinated or divergent selection, or ‘internal’ processes, like developmental coupling among brain regions. Although these hypotheses are not mutually exclusive, there is little agreement over their relative importance across time or how that importance may vary across evolutionary contexts. Results We introduce an agent-based model to simulate brain evolution in a ‘bare-bones’ system and examine dependencies between variables shaping brain evolution. We show that ‘concerted’ patterns of brain evolution do not, in themselves, provide evidence for developmental coupling, despite these terms often being treated as synonymous in the literature. Instead, concerted evolution can reflect either functional or developmental integration. Our model further allows us to clarify conditions under which such developmental coupling, or uncoupling, is potentially adaptive, revealing support for the maintenance of both mechanisms in neural evolution. Critically, we illustrate how the probability of deviation from concerted evolution depends on the cost/benefit ratio of neural tissue, which increases when overall brain size is itself under constraint. Conclusions We conclude that both developmentally coupled and uncoupled brain architectures can provide adaptive mechanisms, depending on the distribution of selection across brain structures, life history and costs of neural tissue. However, when constraints also act on overall brain size, heterogeneity in selection across brain structures will favour region specific, or mosaic, evolution. Regardless, the respective advantages of developmentally coupled and uncoupled brain architectures mean that both may persist in fluctuating environments. This implies that developmental coupling is unlikely to be a persistent constraint, but could evolve as an adaptive outcome to selection to maintain functional integration.https://doi.org/10.1186/s12915-021-01024-1Brain structureBrain sizeConstraintConcerted evolutionMosaic evolutionNeuro-evo-devo
spellingShingle Shahar Avin
Adrian Currie
Stephen H. Montgomery
An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution
BMC Biology
Brain structure
Brain size
Constraint
Concerted evolution
Mosaic evolution
Neuro-evo-devo
title An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution
title_full An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution
title_fullStr An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution
title_full_unstemmed An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution
title_short An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution
title_sort agent based model clarifies the importance of functional and developmental integration in shaping brain evolution
topic Brain structure
Brain size
Constraint
Concerted evolution
Mosaic evolution
Neuro-evo-devo
url https://doi.org/10.1186/s12915-021-01024-1
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