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

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

10.1101/2021.09.29.462233 ◽

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.

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Brain regions associated with visual cues are important for bird migration

Biology Letters ◽

10.1098/rsbl.2015.0678 ◽

2015 ◽

Vol 11 (11) ◽

pp. 20150678 ◽

Cited By ~ 11

Author(s):

Orsolya Vincze ◽

Csongor I. Vágási ◽

Péter L. Pap ◽

Gergely Osváth ◽

Anders Pape Møller

Keyword(s):

Visual Cues ◽

Optic Lobe ◽

Brain Size ◽

Relative Size ◽

Bird Species ◽

Interspecific Variation ◽

Brain Regions ◽

Long Distance ◽

Migration Distance ◽

Whole Brain

Long-distance migratory birds have relatively smaller brains than short-distance migrants or residents. Here, we test whether reduction in brain size with migration distance can be generalized across the different brain regions suggested to play key roles in orientation during migration. Based on 152 bird species, belonging to 61 avian families from six continents, we show that the sizes of both the telencephalon and the whole brain decrease, and the relative size of the optic lobe increases, while cerebellum size does not change with increasing migration distance. Body mass, whole brain size, optic lobe size and wing aspect ratio together account for a remarkable 46% of interspecific variation in average migration distance across bird species. These results indicate that visual acuity might be a primary neural adaptation to the ecological challenge of migration.

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Selection for reduced fear in red junglefowl changes brain composition and affects fear memory

Royal Society Open Science ◽

10.1098/rsos.200628 ◽

2020 ◽

Vol 7 (8) ◽

pp. 200628

Author(s):

Rebecca Katajamaa ◽

Per Jensen

Keyword(s):

Body Size ◽

Brain Size ◽

Prior Experience ◽

Fear Memory ◽

Brain Regions ◽

Preference Learning ◽

Response To Selection ◽

Red Junglefowl ◽

Selection For ◽

Region Size

Brain size reduction is a common trait in domesticated species when compared to wild conspecifics. This reduction can happen through changes in individual brain regions as a response to selection on specific behaviours. We selected red junglefowl for 10 generations for diverging levels of fear towards humans and measured brain size and composition as well as habituation learning and conditioned place preference learning in young chicks. Brain size relative to body size as well as brainstem region size relative to whole brain size were significantly smaller in chicks selected for low fear of humans compared to chicks selected for high fear of humans. However, when including allometric effects in the model, these differences disappear but a tendency towards larger cerebra in low-fear chickens remains. Low-fear line chicks habituated more effectively to a fearful stimulus with prior experience of that same stimulus, whereas high-fear line chicks with previous experience of the stimulus had a response similar to naive chicks. The phenotypical changes are in line with previously described effects of domestication.

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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)

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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Predation impacts brain allometry and offspring production in female guppies (Poecilia reticulata)

10.32942/osf.io/3cxue ◽

2021 ◽

Author(s):

Regina Vega-Trejo ◽

David Joseph Mitchell ◽

Catarina Vila Pouca ◽

Alexander Kotrschal

Keyword(s):

Poecilia Reticulata ◽

Brain Size ◽

Relative Size ◽

Reproductive Traits ◽

Brain Evolution ◽

Predation Pressure ◽

Control Fish ◽

Brain Anatomy ◽

Offspring Production ◽

The Impact

Survivorship under predation exerts strong selection on reproductive traits as well as on brain anatomy of prey. However, how exactly predation and brain evolution are linked has not been resolved as current empirical evidence is inconclusive. This may be due to predation pressure having different effects across life stages and/or due to confounding factors in ecological comparisons of predation pressure. Here, we used adult guppies (Poecilia reticulata) to experimentally test the impact of a period of strong predation on brain anatomy and reproduction of surviving individuals. We compared the survivors to control fish, which were exposed to visual and olfactory predator cues but could not be predated on, and found that predation impacted the relative size of female brains. This effect was dependent on body size as larger female survivors showed relatively larger brains, while smaller survivors showed relatively smaller brains when compared to control animals. There were no differences in male relative brain size between the treatments, nor for any specific relative brain region sizes for either sex. Moreover, survivors produced more offspring, but did not show shorter interbrood intervals than controls. Our results corroborate the important, yet complex, role of predation as an important factor behind variation in brain anatomy.

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Feeding specialization and longer generation time are associated with relatively larger brains in bees

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.0762 ◽

2020 ◽

Vol 287 (1935) ◽

pp. 20200762

Author(s):

Ferran Sayol ◽

Miguel Á. Collado ◽

Joan Garcia-Porta ◽

Marc A. Seid ◽

Jason Gibbs ◽

...

Keyword(s):

Body Size ◽

Brain Size ◽

Phylogenetic Reconstruction ◽

Brain Evolution ◽

Insect Brain ◽

Substantial Variation ◽

Selective Pressures ◽

Feeding Specialization ◽

Relative Brain Size ◽

Insect Group

Despite their miniature brains, insects exhibit substantial variation in brain size. Although the functional significance of this variation is increasingly recognized, research on whether differences in insect brain sizes are mainly the result of constraints or selective pressures has hardly been performed. Here, we address this gap by combining prospective and retrospective phylogenetic-based analyses of brain size for a major insect group, bees (superfamily Apoidea). Using a brain dataset of 93 species from North America and Europe, we found that body size was the single best predictor of brain size in bees. However, the analyses also revealed that substantial variation in brain size remained even when adjusting for body size. We consequently asked whether such variation in relative brain size might be explained by adaptive hypotheses. We found that ecologically specialized species with single generations have larger brains—relative to their body size—than generalist or multi-generation species, but we did not find an effect of sociality on relative brain size. Phylogenetic reconstruction further supported the existence of different adaptive optima for relative brain size in lineages differing in feeding specialization and reproductive strategy. Our findings shed new light on the evolution of the insect brain, highlighting the importance of ecological pressures over social factors and suggesting that these pressures are different from those previously found to influence brain evolution in other taxa.

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Neocortex expansion is linked to size variations in gene families with chemotaxis, cell–cell signalling and immune response functions in mammals

Open Biology ◽

10.1098/rsob.160132 ◽

2016 ◽

Vol 6 (10) ◽

pp. 160132

Author(s):

Atahualpa Castillo-Morales ◽

Jimena Monzón-Sandoval ◽

Alexandra A. de Sousa ◽

Araxi O. Urrutia ◽

Humberto Gutierrez

Keyword(s):

Immune Response ◽

Adult Development ◽

Brain Size ◽

Mammalian Species ◽

Cell Signalling ◽

Relative Size ◽

Brain Evolution ◽

Gene Families ◽

Evolutionary Innovation ◽

Cell Cell

Increased brain size is thought to have played an important role in the evolution of mammals and is a highly variable trait across lineages. Variations in brain size are closely linked to corresponding variations in the size of the neocortex, a distinct mammalian evolutionary innovation. The genomic features that explain and/or accompany variations in the relative size of the neocortex remain unknown. By comparing the genomes of 28 mammalian species, we show that neocortical expansion relative to the rest of the brain is associated with variations in gene family size (GFS) of gene families that are significantly enriched in biological functions associated with chemotaxis, cell–cell signalling and immune response. Importantly, we find that previously reported GFS variations associated with increased brain size are largely accounted for by the stronger link between neocortex expansion and variations in the size of gene families. Moreover, genes within these families are more prominently expressed in the human neocortex during early compared with adult development. These results suggest that changes in GFS underlie morphological adaptations during brain evolution in mammalian lineages.

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Précis of Principles of Brain Evolution

Behavioral and Brain Sciences ◽

10.1017/s0140525x06009010 ◽

2006 ◽

Vol 29 (1) ◽

pp. 1-12 ◽

Cited By ~ 69

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.

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