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

BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Shahar Avin ◽  
Adrian Currie ◽  
Stephen H. Montgomery
Keyword(s):  
Concerted Evolution ◽  
Brain Size ◽  
Functional Integration ◽  
Cost Benefit ◽  
Brain Evolution ◽  
Neural Tissue ◽  
Brain Structures ◽  
Brain Regions ◽  
Agent Based Model ◽  
Agent Based

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.

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

2020 ◽  
Author(s):  
Shahar Avin ◽  
Adrian Currie ◽  
Stephen H. Montgomery
Keyword(s):  
Brain Structure ◽  
Brain Evolution ◽  
Brain Regions ◽  
Phenotypic Change ◽  
Evolutionary Constraint ◽  
Agent Based Model ◽  
Variable Environment ◽  
Relative Significance ◽  
Agent Based ◽  
Vertebrate Brain

AbstractComparisons of vertebrate brain structure suggest a conserved pattern of scaling between components, but also many examples of lineages diverging dramatically from these general trends. Two competing hypotheses of brain evolution seek to explain these patterns of variation by invoking either ‘external’ processes, such as selection driving phenotypic change, or ‘internal’ processes, like developmental coupling among brain regions. Efforts to reconcile these views remain deadlocked, in part due to empirical under-determination and the limitations of ‘relative significance’ debates. We introduce an agent-based model that allows us to simulate brain evolution in a ‘bare-bones’ system and examine the dependencies between variables that may shape brain evolution. Our simulations formalise verbal arguments and interpretations concerning the evolution of brain structure. We illustrate that ‘concerted’ patterns of brain evolution cannot alone be taken as evidence for developmental coupling, or constraint, despite these terms often being treated as synonymous in the literature. Both developmentally coupled and uncoupled brain architectures can represent adaptive mechanisms, depending on the distribution of selection across the brain, life history, and the relative costs of neural tissue. Our model also illustrates how the prevalence of mosaic and concerted patterns of evolution may fluctuate through time in a variable environment, which we argue implies that developmental coupling is unlikely to be a significant evolutionary constraint.

scholarly journals Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes

2021 ◽  
Author(s):  
Erika L. Schumacher ◽  
Bruce A. Carlson
Keyword(s):  
Brain Region ◽  
Brain Size ◽  
Brain Evolution ◽  
Brain Regions ◽  
Torus Semicircularis ◽  
Micro Computed Tomography ◽  
Electrosensory System ◽  
Electric Fishes ◽  
Weakly Electric ◽  
Region Size

AbstractBrain region size generally scales allometrically with total brain size, but mosaic shifts in brain region size independent of brain size have been found in several lineages and may be related to the evolution of behavioral novelty. African weakly electric fishes (Mormyroidea) evolved a mosaically enlarged cerebellum and hindbrain, yet the relationship to their behaviorally novel electrosensory system remains unclear. We addressed this by studying South American weakly electric fishes (Gymnotiformes) and weakly electric catfishes (Synodontis spp.), which evolved varying aspects of electrosensory systems, independent of mormyroids. If the mormyroid mosaic increases are related to evolving an electrosensory system, we should find similar mosaic shifts in gymnotiforms and Synodontis. Using micro-computed tomography scans, we quantified brain region scaling for multiple electrogenic, electroreceptive, and non-electrosensing species. We found mosaic increases in cerebellum in all three electrogenic lineages relative to non-electric lineages and mosaic increases in torus semicircularis and hindbrain associated with the evolution of electrogenesis and electroreceptor type. These results show that evolving novel electrosensory systems is repeatedly and independently associated with changes in the sizes of individual brain regions independent of brain size, which suggests that selection can impact structural brain composition to favor specific regions involved in novel behaviors.

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

2015 ◽  
Vol 282 (1810) ◽  
pp. 20151008 ◽  
Author(s):  
Kristina Noreikiene ◽  
Gábor Herczeg ◽  
Abigél Gonda ◽  
Gergely Balázs ◽  
Arild Husby ◽  
...  
Keyword(s):  
Body Size ◽  
Brain Size ◽  
Additive Genetic Variance ◽  
Genetic Correlations ◽  
Relative Size ◽  
Strong Support ◽  
Brain Evolution ◽  
Brain Regions ◽  
Independent Evolution ◽  
Mosaic Model

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 h 2 = 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 r G = 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 ( r G = 0.89), suggesting a constraint for independent evolution of brain and body size in sticklebacks.

scholarly journals Maternal investment, life histories and the evolution of brain structure in primates

2019 ◽  
Vol 286 (1911) ◽  
pp. 20191608 ◽  
Author(s):  
Lauren E. Powell ◽  
Robert A. Barton ◽  
Sally E. Street
Keyword(s):  
Life History ◽  
Life Histories ◽  
Brain Size ◽  
Developmental Trajectories ◽  
Adult Life ◽  
Maternal Investment ◽  
Brain Evolution ◽  
Brain Structures ◽  
Juvenile Period ◽  
Adult Lifespan

Life history is a robust correlate of relative brain size: larger-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. The cognitive buffer hypothesis (CBH) proposes an adaptive explanation for this relationship: large brains may permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing for reduced mortality and increased lifespan. By contrast, the developmental costs hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains, predicting correlations with pre-adult life-history phases. Here, we test novel predictions of the hypotheses in primates applied to the neocortex and cerebellum, two major brain structures with distinct developmental trajectories. While neocortical growth is allocated primarily to pre-natal development, the cerebellum exhibits relatively substantial post-natal growth. Consistent with the DCH, neocortical expansion is related primarily to extended gestation while cerebellar expansion to extended post-natal development, particularly the juvenile period. Contrary to the CBH, adult lifespan explains relatively little variance in the whole brain or neocortex volume once pre-adult life-history phases are accounted for. Only the cerebellum shows a relationship with lifespan after accounting for developmental periods. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental phases, and imply that environmental input during post-natal maturation may be particularly crucial for the development of cerebellar function. They also suggest that relatively extended post-natal maturation times provide a developmental mechanism for the marked expansion of the cerebellum in the apes.

scholarly journals Rapid mosaic brain evolution under artificial selection for relative telencephalon size in the guppy (Poecilia reticulata)

2021 ◽  
Author(s):  
Stephanie Fong ◽  
Björn Rogell ◽  
Mirjam Amcoff ◽  
Alexander Kotrschal ◽  
Wouter van der Bijl ◽  
...  
Keyword(s):  
Artificial Selection ◽  
Poecilia Reticulata ◽  
Brain Size ◽  
Brain Evolution ◽  
Brain Regions ◽  
Research Field ◽  
Selected Lines ◽  
Vertebrate Brain ◽  
Offspring Production ◽  
Mosaic Brain Evolution

The vertebrate brain displays enormous morphological variation and the quest to understand the evolutionary causes and consequences of this variation has spurred much research. The mosaic brain evolution hypothesis, stating that brain regions can evolve relatively independently, is an important idea in this research field. Here we provide experimental support for this hypothesis through an artificial selection experiment in the guppy (Poecilia reticulata). After four generations of selection on relative telencephalon volume (relative to brain size) in replicated up-selected, down-selected and control-lines, we found substantial changes in telencephalon size, but no changes in other regions. Comparisons revealed that up-selected lines had larger telencephalon while down-selected lines had smaller telencephalon than wild Trinidadian populations. No cost of increasing telencephalon size was detected in offspring production. Our results support that independent evolutionary changes in specific brain regions through mosaic brain evolution can be important facilitators of cognitive evolution.

scholarly journals Relative Brain Size and Its Relation with the Associative Pallium in Birds

2016 ◽  
Vol 87 (2) ◽  
pp. 69-77 ◽  
Author(s):  
Ferran Sayol ◽  
Louis Lefebvre ◽  
Daniel Sol
Keyword(s):  
Brain Size ◽  
Large Fraction ◽  
Biological Significance ◽  
Size Variation ◽  
Brain Structures ◽  
Brain Regions ◽  
Whole Brain ◽  
Small Areas ◽  
Mosaic Evolution ◽  
The Brain

Despite growing interest in the evolution of enlarged brains, the biological significance of brain size variation remains controversial. Much of the controversy is over the extent to which brain structures have evolved independently of each other (mosaic evolution) or in a coordinated way (concerted evolution). If larger brains have evolved by the increase of different brain regions in different species, it follows that comparisons of the whole brain might be biologically meaningless. Such an argument has been used to criticize comparative attempts to explain the existing variation in whole-brain size among species. Here, we show that pallium areas associated with domain-general cognition represent a large fraction of the entire brain, are disproportionally larger in large-brained birds and accurately predict variation in the whole brain when allometric effects are appropriately accounted for. While this does not question the importance of mosaic evolution, it suggests that examining specialized, small areas of the brain is not very helpful for understanding why some birds have evolved such large brains. Instead, the size of the whole brain reflects consistent variation in associative pallium areas and hence is functionally meaningful for comparative analyses.

Developmental structure in brain evolution

2001 ◽  
Vol 24 (2) ◽  
pp. 263-278 ◽  
Author(s):  
Barbara L. Finlay ◽  
Richard B. Darlington ◽  
Nicholas Nicastro
Keyword(s):  
Large Scale ◽  
Mammalian Species ◽  
Brain Evolution ◽  
Brain Structures ◽  
Brain Regions ◽  
Structural Constraints ◽  
Thalamic Nuclei ◽  
Brain Expansion ◽  
A Minor ◽  
Selection Of

How does evolution grow bigger brains? It has been widely assumed that growth of individual structures and functional systems in response to niche-specific cognitive challenges is the most plausible mechanism for brain expansion in mammals. Comparison of multiple regressions on allometric data for 131 mammalian species, however, suggests that for 9 of 11 brain structures taxonomic and body size factors are less important than covariance of these major structures with each other. Which structure grows biggest is largely predicted by a conserved order of neurogenesis that can be derived from the basic axial structure of the developing brain. This conserved order of neurogenesis predicts the relative scaling not only of gross brain regions like the isocortex or mesencephalon, but also the level of detail of individual thalamic nuclei. Special selection of particular areas for specific functions does occur, but it is a minor factor compared to the large-scale covariance of the whole brain. The idea that enlarged isocortex could be a “spandrel,” a by-product of structural constraints later adapted for various behaviors, contrasts with approaches to selection of particular brain regions for cognitively advanced uses, as is commonly assumed in the case of hominid brain evolution.

Neuroanatomical and Morphological Trait Clusters in the Ant Genus Pheidole: Evidence for Modularity and Integration in Brain Structure

2015 ◽  
Vol 85 (1) ◽  
pp. 63-76 ◽  
Author(s):  
Iulian Ilieş ◽  
Mario L. Muscedere ◽  
James F.A. Traniello
Keyword(s):  
Social Information Processing ◽  
Brain Structure ◽  
Developmental Trajectories ◽  
Size Variation ◽  
Brain Evolution ◽  
Brain Structures ◽  
Interspecific Variation ◽  
Distinct Species ◽  
Brain Regions ◽  
Brain Organization

A central question in brain evolution concerns how selection has structured neuromorphological variation to generate adaptive behavior. In social insects, brain structures differ between reproductive and sterile castes, and worker behavioral specializations related to morphology, age, and ecology are associated with intra- and interspecific variation in investment in functionally different brain compartments. Workers in the hyperdiverse ant genus Pheidole are morphologically and behaviorally differentiated into minor and major subcastes that exhibit distinct species-typical patterns of brain compartment size variation. We examined integration and modularity in brain organization and its developmental patterning in three ecotypical Pheidole species by analyzing intra- and interspecific morphological and neuroanatomical covariation. Our results identified two trait clusters, the first involving olfaction and social information processing and the second composed of brain regions regulating nonolfactory sensorimotor functions. Patterns of size covariation between brain compartments within subcastes were consistent with levels of behavioral differentiation between minor and major workers. Globally, brains of mature workers were more heterogeneous than brains of newly eclosed workers, suggesting diversified developmental trajectories underscore species- and subcaste-typical brain organization. Variation in brain structure associated with the striking worker polyphenism in our sample of Pheidole appears to originate from initially differentiated brain templates that further diverge through species- and subcaste-specific processes of maturation and behavioral development.

Précis of Principles of Brain Evolution

2006 ◽  
Vol 29 (1) ◽  
pp. 1-12 ◽  
Author(s):  
Georg F. Striedter
Keyword(s):  
Brain Structure ◽  
Homo Sapiens ◽  
Brain Size ◽  
Brain Evolution ◽  
Detailed Examination ◽  
Brain Regions ◽  
Impact Function ◽  
Neuronal Connections ◽  
Rules And Principles ◽  
Using Data

Brain evolution is a complex weave of species similarities and differences, bound by diverse rules and principles. This book is a detailed examination of these principles, using data from a wide array of vertebrates but minimizing technical details and terminology. It is written for advanced undergraduates, graduate students, and more senior scientists who already know something about “the brain,” but want a deeper understanding of how diverse brains evolved. The book's central theme is that evolutionary changes in absolute brain size tend to correlate with many other aspects of brain structure and function, including the proportional size of individual brain regions, their complexity, and their neuronal connections. To explain these correlations, the book delves into rules of brain development and asks how changes in brain structure impact function and behavior. Two chapters focus specifically on how mammal brains diverged from other brains and how Homo sapiens evolved a very large and “special” brain.

scholarly journals Why big brains? A comparison of models for both primate and carnivore brain size evolution

PLoS ONE ◽  
2021 ◽  
Vol 16 (12) ◽  
pp. e0261185
Author(s):  
Helen Rebecca Chambers ◽  
Sandra Andrea Heldstab ◽  
Sean J. O’Hara
Keyword(s):  
Life History ◽  
Brain Size ◽  
Size Variation ◽  
Ecological Factors ◽  
Brain Evolution ◽  
Brain Regions ◽  
Home Range Size ◽  
Careful Consideration ◽  
Social Brain ◽  
Multiple Variables

Despite decades of research, much uncertainty remains regarding the selection pressures responsible for brain size variation. Whilst the influential social brain hypothesis once garnered extensive support, more recent studies have failed to find support for a link between brain size and sociality. Instead, it appears there is now substantial evidence suggesting ecology better predicts brain size in both primates and carnivores. Here, different models of brain evolution were tested, and the relative importance of social, ecological, and life-history traits were assessed on both overall encephalisation and specific brain regions. In primates, evidence is found for consistent associations between brain size and ecological factors, particularly diet; however, evidence was also found advocating sociality as a selection pressure driving brain size. In carnivores, evidence suggests ecological variables, most notably home range size, are influencing brain size; whereas, no support is found for the social brain hypothesis, perhaps reflecting the fact sociality appears to be limited to a select few taxa. Life-history associations reveal complex selection mechanisms to be counterbalancing the costs associated with expensive brain tissue through extended developmental periods, reduced fertility, and extended maximum lifespan. Future studies should give careful consideration of the methods chosen for measuring brain size, investigate both whole brain and specific brain regions where possible, and look to integrate multiple variables, thus fully capturing all of the potential factors influencing brain size.

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