Limits...
Brain scaling in mammalian evolution as a consequence of concerted and mosaic changes in numbers of neurons and average neuronal cell size.

Herculano-Houzel S, Manger PR, Kaas JH - Front Neuroanat (2014)

Bottom Line: Based on an analysis of the shared and clade-specific characteristics of 41 modern mammalian species in 6 clades, and in light of the phylogenetic relationships among them, here we propose that ancestral mammal brains were composed and scaled in their cellular composition like modern afrotherian and glire brains: with an addition of neurons that is accompanied by a decrease in neuronal density and very little modification in glial cell density, implying a significant increase in average neuronal cell size in larger brains, and the allocation of approximately 2 neurons in the cerebral cortex and 8 neurons in the cerebellum for every neuron allocated to the rest of brain.We also propose that in some clades the scaling of different brain structures has diverged away from the common ancestral layout through clade-specific (or clade-defining) changes in how average neuronal cell mass relates to numbers of neurons in each structure, and how numbers of neurons are differentially allocated to each structure relative to the number of neurons in the rest of brain.Thus, the evolutionary expansion of mammalian brains has involved both concerted and mosaic patterns of scaling across structures.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro Rio de Janeiro, Brazil ; Instituto Nacional de Neurociência Translacional, Ministério de Ciência e Tecnologia São Paulo, Brazil.

ABSTRACT
Enough species have now been subject to systematic quantitative analysis of the relationship between the morphology and cellular composition of their brain that patterns begin to emerge and shed light on the evolutionary path that led to mammalian brain diversity. Based on an analysis of the shared and clade-specific characteristics of 41 modern mammalian species in 6 clades, and in light of the phylogenetic relationships among them, here we propose that ancestral mammal brains were composed and scaled in their cellular composition like modern afrotherian and glire brains: with an addition of neurons that is accompanied by a decrease in neuronal density and very little modification in glial cell density, implying a significant increase in average neuronal cell size in larger brains, and the allocation of approximately 2 neurons in the cerebral cortex and 8 neurons in the cerebellum for every neuron allocated to the rest of brain. We also propose that in some clades the scaling of different brain structures has diverged away from the common ancestral layout through clade-specific (or clade-defining) changes in how average neuronal cell mass relates to numbers of neurons in each structure, and how numbers of neurons are differentially allocated to each structure relative to the number of neurons in the rest of brain. Thus, the evolutionary expansion of mammalian brains has involved both concerted and mosaic patterns of scaling across structures. This is, to our knowledge, the first mechanistic model that explains the generation of brains large and small in mammalian evolution, and it opens up new horizons for seeking the cellular pathways and genes involved in brain evolution.

No MeSH data available.


Phylogenetic relationships among the 41 species analyzed. Tree compiled according to Price et al. (2005); Purvis (1995); Blanga-Kanfi et al. (2009); Douady et al. (2002); Shinohara et al. (2003). The same color code identifying clades is used throughout the figures. Estimated times of divergence across clades (asterisks) are indicated, according to Murphy et al. (2004).
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Figure 1: Phylogenetic relationships among the 41 species analyzed. Tree compiled according to Price et al. (2005); Purvis (1995); Blanga-Kanfi et al. (2009); Douady et al. (2002); Shinohara et al. (2003). The same color code identifying clades is used throughout the figures. Estimated times of divergence across clades (asterisks) are indicated, according to Murphy et al. (2004).

Mentions: Our dataset includes the cerebral cortex (both gray and white matter combined), the cerebellum (including the deep nuclei), the olfactory bulb and the rest of brain (the ensemble of brainstem, diencephalon and striatum). We analyze a total of 41 species, whose phylogenetic relationships are shown in Figure 1. Our data include 5 afrotherians (Neves et al., 2014), 10 glires (Herculano-Houzel et al., 2006, 2011), 15 primates (including humans; Herculano-Houzel et al., 2007; Azevedo et al., 2009; Gabi et al., 2010), 5 eulipotyphlans (Sarko et al., 2009), 1 scandentia (Herculano-Houzel et al., 2007) and 5 artiodactyls (Kazu et al., under review). Afrotherians are an important group for the phylogenetic analysis of brain scaling due to their basal branching between 100 and 110 million years ago from the lineages that gave rise to laurasiatherians (artiodactyls and eulipotyphlans, in our sample) and to euarchontoglires (rodents, lagomorphs, scandentia and primates; Murphy et al., 2004). Laurasiatherians and euarchontoglires diverged 90–100 million years ago, and within each of them, both artiodactyls and eulipotyphlans, and glires and primates, branched off around 90 million years ago (Murphy et al.; Figure 1). Thus, although our analysis at present excludes carnivores, perissodactyls, chiropterans, and cetaceans (although the latter belong to the order Cetartiodactyla, which includes the artiodactyls examined here), all these clades are part of Laurasiatheria; Xenarthra is the only major independent branch of eutherians that is missing in our analysis.


Brain scaling in mammalian evolution as a consequence of concerted and mosaic changes in numbers of neurons and average neuronal cell size.

Herculano-Houzel S, Manger PR, Kaas JH - Front Neuroanat (2014)

Phylogenetic relationships among the 41 species analyzed. Tree compiled according to Price et al. (2005); Purvis (1995); Blanga-Kanfi et al. (2009); Douady et al. (2002); Shinohara et al. (2003). The same color code identifying clades is used throughout the figures. Estimated times of divergence across clades (asterisks) are indicated, according to Murphy et al. (2004).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4127475&req=5

Figure 1: Phylogenetic relationships among the 41 species analyzed. Tree compiled according to Price et al. (2005); Purvis (1995); Blanga-Kanfi et al. (2009); Douady et al. (2002); Shinohara et al. (2003). The same color code identifying clades is used throughout the figures. Estimated times of divergence across clades (asterisks) are indicated, according to Murphy et al. (2004).
Mentions: Our dataset includes the cerebral cortex (both gray and white matter combined), the cerebellum (including the deep nuclei), the olfactory bulb and the rest of brain (the ensemble of brainstem, diencephalon and striatum). We analyze a total of 41 species, whose phylogenetic relationships are shown in Figure 1. Our data include 5 afrotherians (Neves et al., 2014), 10 glires (Herculano-Houzel et al., 2006, 2011), 15 primates (including humans; Herculano-Houzel et al., 2007; Azevedo et al., 2009; Gabi et al., 2010), 5 eulipotyphlans (Sarko et al., 2009), 1 scandentia (Herculano-Houzel et al., 2007) and 5 artiodactyls (Kazu et al., under review). Afrotherians are an important group for the phylogenetic analysis of brain scaling due to their basal branching between 100 and 110 million years ago from the lineages that gave rise to laurasiatherians (artiodactyls and eulipotyphlans, in our sample) and to euarchontoglires (rodents, lagomorphs, scandentia and primates; Murphy et al., 2004). Laurasiatherians and euarchontoglires diverged 90–100 million years ago, and within each of them, both artiodactyls and eulipotyphlans, and glires and primates, branched off around 90 million years ago (Murphy et al.; Figure 1). Thus, although our analysis at present excludes carnivores, perissodactyls, chiropterans, and cetaceans (although the latter belong to the order Cetartiodactyla, which includes the artiodactyls examined here), all these clades are part of Laurasiatheria; Xenarthra is the only major independent branch of eutherians that is missing in our analysis.

Bottom Line: Based on an analysis of the shared and clade-specific characteristics of 41 modern mammalian species in 6 clades, and in light of the phylogenetic relationships among them, here we propose that ancestral mammal brains were composed and scaled in their cellular composition like modern afrotherian and glire brains: with an addition of neurons that is accompanied by a decrease in neuronal density and very little modification in glial cell density, implying a significant increase in average neuronal cell size in larger brains, and the allocation of approximately 2 neurons in the cerebral cortex and 8 neurons in the cerebellum for every neuron allocated to the rest of brain.We also propose that in some clades the scaling of different brain structures has diverged away from the common ancestral layout through clade-specific (or clade-defining) changes in how average neuronal cell mass relates to numbers of neurons in each structure, and how numbers of neurons are differentially allocated to each structure relative to the number of neurons in the rest of brain.Thus, the evolutionary expansion of mammalian brains has involved both concerted and mosaic patterns of scaling across structures.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro Rio de Janeiro, Brazil ; Instituto Nacional de Neurociência Translacional, Ministério de Ciência e Tecnologia São Paulo, Brazil.

ABSTRACT
Enough species have now been subject to systematic quantitative analysis of the relationship between the morphology and cellular composition of their brain that patterns begin to emerge and shed light on the evolutionary path that led to mammalian brain diversity. Based on an analysis of the shared and clade-specific characteristics of 41 modern mammalian species in 6 clades, and in light of the phylogenetic relationships among them, here we propose that ancestral mammal brains were composed and scaled in their cellular composition like modern afrotherian and glire brains: with an addition of neurons that is accompanied by a decrease in neuronal density and very little modification in glial cell density, implying a significant increase in average neuronal cell size in larger brains, and the allocation of approximately 2 neurons in the cerebral cortex and 8 neurons in the cerebellum for every neuron allocated to the rest of brain. We also propose that in some clades the scaling of different brain structures has diverged away from the common ancestral layout through clade-specific (or clade-defining) changes in how average neuronal cell mass relates to numbers of neurons in each structure, and how numbers of neurons are differentially allocated to each structure relative to the number of neurons in the rest of brain. Thus, the evolutionary expansion of mammalian brains has involved both concerted and mosaic patterns of scaling across structures. This is, to our knowledge, the first mechanistic model that explains the generation of brains large and small in mammalian evolution, and it opens up new horizons for seeking the cellular pathways and genes involved in brain evolution.

No MeSH data available.