Genetic architecture supports mosaic brain evolution and independent brain–body size regulation

The 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 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.

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Faculty Opinions recommendation of Growth-Blocking Peptides As Nutrition-Sensitive Signals for Insulin Secretion and Body Size Regulation.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.726183129.793516553 ◽

2016 ◽

Author(s):

Savraj Grewal

Keyword(s):

Insulin Secretion ◽

Body Size ◽

Size Regulation ◽

Nutrition Sensitive

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Allometry unleashed: an adaptationist approach of brain scaling in mammalian evolution

10.7287/peerj.preprints.27872 ◽

2019 ◽

Cited By ~ 1

Author(s):

Romain Willemet

Keyword(s):

Body Size ◽

Allometric Scaling ◽

Species Differences ◽

Brain Size ◽

Brain Evolution ◽

Neural Systems ◽

Selection Pressures ◽

Number Of Factors ◽

Functional Consequences ◽

Main Factor

The idea that allometry in the context of brain evolution mainly result from constraints channelling the scaling of brain components is deeply embedded in the field of comparative neurobiology. Constraints, however, only prevent or limit changes, and cannot explain why these changes happen in the first place. In fact, considering allometry as a lack of change may be one of the reasons why, after more than a century of research, there is still no satisfactory explanatory framework for the understanding of species differences in brain size and composition in mammals. The present paper attempts to tackle this issue by adopting an adaptationist approach to examine the factors behind the evolution of brain components. In particular, the model presented here aims to explain the presence of patterns of covariation among brain components found within major taxa, and the differences between taxa. The key determinant of these patterns of covariation within a taxon-cerebrotype (groups of species whose brains present a number of similarities at the physiological and anatomical levels) seems to be the presence of taxon-specific patterns of selection pressures targeting the functional and structural properties of neural components or systems. Species within a taxon share most of the selection pressures, but their levels scale with a number of factors that are often related to body size. The size and composition of neural systems respond to these selection pressures via a number of evolutionary scenarios, which are discussed here. Adaptation, rather than, as generally assumed, developmental or functional constraints, thus appears to be the main factor behind the allometric scaling of brain components. The fact that the selection pressures acting on the size of brain components form a pattern that is specific to each taxon accounts for the peculiar relationship between body size, brain size and composition, and behavioural capabilities characterizing each taxon. While it is important to avoid repeating the errors of the “Panglossian paradigm”, the elements presented here suggests that an adaptationist approach may shed a new light on the factors underlying, and the functional consequences of, species differences in brain size and composition.

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WHATEVER YOU WANT: INCONSISTENT RESULTS IS THE RULE, NOT THE EXCEPTION, IN THE STUDY OF PRIMATE BRAIN EVOLUTION

10.1101/454132 ◽

2018 ◽

Cited By ~ 1

Author(s):

Andreas Wartel ◽

Patrik Lindenfors ◽

Johan Lind

Keyword(s):

Body Size ◽

Brain Evolution ◽

Data Sets ◽

Data Set ◽

Scientific Rigor ◽

Explanatory Variables ◽

Primate Brain ◽

Residual Variation ◽

The Many ◽

Brain Data

AbstractPrimate brains differ in size and architecture. Hypotheses to explain this variation are numerous and many tests have been carried out. However, after body size has been accounted for there is little left to explain. The proposed explanatory variables for the residual variation are many and covary, both with each other and with body size. Further, the data sets used in analyses have been small, especially in light of the many proposed predictors. Here we report the complete list of models that results from exhaustively combining six commonly used predictors of brain and neocortex size. This provides an overview of how the output from standard statistical analyses changes when the inclusion of different predictors is altered. By using both the most commonly tested brain data set and a new, larger data set, we show that the choice of included variables fundamentally changes the conclusions as to what drives primate brain evolution. Our analyses thus reveal why studies have had troubles replicating earlier results and instead have come to such different conclusions. Although our results are somewhat disheartening, they highlight the importance of scientific rigor when trying to answer difficult questions. It is our position that there is currently no empirical justification to highlight any particular hypotheses, of those adaptive hypotheses we have examined here, as the main determinant of primate brain evolution.

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

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.1008 ◽

2015 ◽

Vol 282 (1810) ◽

pp. 20151008 ◽

Cited By ~ 25

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.

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THE GENETIC ARCHITECTURE OF WING SIZE DIVERGENCE AT VARYING SPATIAL SCALES ALONG A BODY SIZE CLINE INDROSOPHILA MELANOGASTER

Evolution ◽

10.1111/j.1558-5646.2010.00975.x ◽

2010 ◽

Author(s):

W. Jason Kennington ◽

Ary A. Hoffmann

Keyword(s):

Body Size ◽

Genetic Architecture ◽

Spatial Scales ◽

Wing Size

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Rethinking the Effects of Body Size on the Study of Brain Size Evolution

Brain Behavior and Evolution ◽

10.1159/000501161 ◽

2019 ◽

Vol 93 (4) ◽

pp. 182-195 ◽

Cited By ~ 4

Author(s):

Enrique Font ◽

Roberto García-Roa ◽

Daniel Pincheira-Donoso ◽

Pau Carazo

Keyword(s):

Body Size ◽

Brain Size ◽

Size Variation ◽

Brain Evolution ◽

Scaling Effects ◽

Selection Pressures ◽

Body Tissues ◽

Relative Brain Size ◽

Functional Components ◽

The Brain

Body size correlates with most structural and functional components of an organism’s phenotype – brain size being a prime example of allometric scaling with animal size. Therefore, comparative studies of brain evolution in vertebrates rely on controlling for the scaling effects of body size variation on brain size variation by calculating brain weight/body weight ratios. Differences in the brain size-body size relationship between taxa are usually interpreted as differences in selection acting on the brain or its components, while selection pressures acting on body size, which are among the most prevalent in nature, are rarely acknowledged, leading to conflicting and confusing conclusions. We address these problems by comparing brain-body relationships from across >1,000 species of birds and non-avian reptiles. Relative brain size in birds is often assumed to be 10 times larger than in reptiles of similar body size. We examine how differences in the specific gravity of body tissues and in body design (e.g., presence/absence of a tail or a dense shell) between these two groups can affect estimates of relative brain size. Using phylogenetic comparative analyses, we show that the gap in relative brain size between birds and reptiles has been grossly exaggerated. Our results highlight the need to take into account differences between taxa arising from selection pressures affecting body size and design, and call into question the widespread misconception that reptile brains are small and incapable of supporting sophisticated behavior and cognition.

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

Science Advances ◽

10.1126/sciadv.abj4314 ◽

2021 ◽

Vol 7 (46) ◽

Author(s):

Stephanie Fong ◽

Björn Rogell ◽

Mirjam Amcoff ◽

Alexander Kotrschal ◽

Wouter van der Bijl ◽

...

Keyword(s):

Artificial Selection ◽

Poecilia Reticulata ◽

Brain Evolution ◽

Selection For ◽

Mosaic Brain Evolution

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

10.1101/2021.03.31.437806 ◽

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.

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Brain evolution: How constrained is it?

Behavioral and Brain Sciences ◽

10.1017/s0140525x01403955 ◽

2001 ◽

Vol 24 (2) ◽

pp. 296-297

Author(s):

Georg F. Striedter

Keyword(s):

Body Size ◽

Brain Evolution ◽

Developmental Constraints ◽

Similar Body ◽

Taxonomic Groups

Allometric analyses suggest that there are some developmental constraints on brain evolution. However, when one compares animals of similar body size, these constraints do not appear to be very tight. Moreover, the constraints often differ between taxonomic groups. Therefore, one may ask not only what causes developmental constraints but also how (and why) these constraints might be altered (or circumvented) during the course of evolution.

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