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Allometry Unleashed: an Adaptationist Approach of Brain Scaling in Mammalian Evolution

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Allometry Unleashed: an Adaptationist Approach of Brain Scaling in Mammalian Evolution Allometry unleashed: an adaptationist approach of brain scaling in mammalian evolution Romain Willemet London, United Kingdom. Email: [email protected] ORCID iD: 0000-0003-4364-3420 Abstract 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. Key-words: allometry; behaviour; brain evolution; brain size; comparative approach PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27872v1 | CC BY 4.0 Open Access | rec: 25 Jul 2019, publ: 25 Jul 2019 Contents Introduction ............................................................................................................................................. 3 1. Comparing brains: the taxon-cerebrotype approach ........................................................................... 5 1.1. Taxon-specific differences........................................................................................................... 5 1.2. Taxon-cerebrotypes and phylogeny ............................................................................................. 7 1.3. Taxon-cerebrotypes and allometry .............................................................................................. 8 2. Interpretations of allometry: constraints and adaptations ................................................................... 9 2.1. Developmental constraints account ............................................................................................. 9 2.2. Functional constraints account .................................................................................................. 11 2.3. A third view: allometry as a pattern of adaptations ................................................................... 13 3. The evolution of functional neural systems ...................................................................................... 14 3.1. Scenarios of concerted evolution within functional neural systems .......................................... 14 3.1.1. Balanced functional selection ............................................................................................. 14 3.1.2. Unbalanced functional selection ........................................................................................ 15 3.1.3. Adjustment effect ............................................................................................................... 16 3.2. Patterns of selection pressures ................................................................................................... 19 4. Factors influencing the evolution of brain size and composition...................................................... 20 4.1. Adaptations and allometry: body size required vs body size allowed adaptations .................... 21 4.2. Functional adaptations ............................................................................................................... 22 4.3. Structural adaptations ................................................................................................................ 28 4.3.1. Body size required adaptations........................................................................................... 28 4.3.2. Body size allowed adaptations ........................................................................................... 30 4.4. Selection pressures acting against an increase in brain component size ................................... 31 4.4.1. Energetic constraints .......................................................................................................... 31 4.4.2. Developmental constraints ................................................................................................. 32 4.5. Summary on the selection factors determining the size of neural components/systems ........... 32 5. A synthesis ........................................................................................................................................ 33 5.1. Understanding differences within and between taxa ................................................................. 33 5.2. Approaches and methods ........................................................................................................... 40 5.2.1. Studying allometry: scaling ................................................................................................ 41 5.2.2. Studying allometry: relative component size ..................................................................... 42 Conclusion ............................................................................................................................................ 45 PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27872v1 | CC BY 4.0 Open Access | rec: 25 Jul 2019, publ: 25 Jul 2019 2 Introduction The remarkable diversity of behaviours displayed by vertebrates has its roots in species differences in brain size and composition. No two species have the same brain, and it is a central goal of the fields of comparative psychology and evolutionary neuroscience to understand the factors behind these differences (Striedter 2005). Overall, the vertebrate brain is composed of a number of anatomically and functionally distinct components (e.g. cortical regions, thalamic nuclei, etc.) that are connected to each other within functionally differentiated neural systems (Nieuwenhuys et al. 1998). Despite the global level of integration between brain components necessary for the brain as a whole to produce adaptive behaviours, individual brain components generally have particular functions that distinguish them from the others (Nieuwenhuys et al. 1998, Healy and Rowe 2007). The functional properties of individual components are determined by their particular physiology and internal structure (Doya 1999) and their pattern of connection to other components (e.g., Behrens et al. 2003, de Schotten et al. 2016). Several factors are responsible for the differentiation of brain components and their evolution. One of them is the existence of selection pressures toward particular brain regions, progressively leading these regions to perform their (potentially new type of) computation at least partly independently from the other components (see Gahr (2000) for an example on the neural song control system in birds). Another factor is the presence of structural constraints, in particular those related to the issue of allowing a given level of connectivity between cells as their number increases, leading to the compartmentalization of neuronal computation as the distance between brain areas increases (Ringo 1991, Kaas 2000), and thereby to the differentiation of brain components. These changes happen in the context of a number of constraints limiting the range of possible outcomes. These are physiological constraints, for example regarding the regulation of energy (e.g. Herculano-Houzel 2014) and connectivity between cells (e.g. Wyatt et al. 2005, Perge et al. 2012), developmental constraints, such as the differential maturation of cells within the brain (e.g., Le Magueresse and Monyer 2013, Yang et al. 2013), and physical constraints, for example in the fact that the brain has to fit within the skull that itself has to be supported by the body (an obvious, but often overlooked factor (Striedter 2005)). PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.27872v1 | CC BY 4.0 Open Access | rec: 25 Jul 2019, publ: 25
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