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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.


Variation in the ratios between numbers of neurons in each structure and numbers of neurons in the rest of brain across clades show a relative increase in numbers of neurons in the cerebral cortex and cerebellum in both primates and artiodactyls. Each symbol represents the average values for the structures indicated in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). (A) Ratio between numbers of neurons in the cerebral cortex and rest of brain is higher in primates (13.58 ± 2.14, red) and artiodactyls (6.96 ± 1.11, pink) than in afrotherians (2.41 ± 0.18, blue), glires (2.11 ± 0.17, green), eulipotyphlans (2.04 ± 0.13, orange) and scandentia (2.69, gray). The arrows and the phylogenetic scheme on the left indicate the divergence of primates and artiodactyls from the ratio shared by afrotherians, eulipotyphlans, scandentia and glires, and thus presumably also by ancestral mammals. (B) Ratio between numbers of neurons in the cerebellum and rest of brain is also higher in primates (35.91 ± 6.95, red) and artiodactyls (37.34 ± 5.72, pink) than in afrotherians (6.88 ± 0.89, blue), glires (10.03 ± 1.05, green), eulipotyphlans (9.14 ± 2.05, orange) and scandentia (8.24, gray). The arrows and the phylogenetic scheme on the left indicate the divergence of primates and artiodactyls from the ratio shared by afrotherians, eulipotyphlans, scandentia and glires, and thus presumably also by ancestral mammals. (C) ratio between numbers of neurons in the olfactory bulb and rest of brain are larger than 1 only in eulipotyphlans (1.52 ± 0.31, orange), compared to 0.65 ± 0.11 in glires, 0.68 ± 0.22 in afrotherians, 0.49 ± 0.27 in primates, 0.56 in scandentia, and 0.23 ± 0.05 in artiodactyls. The arrows and the phylogenetic scheme on the left indicate the divergence of eulipotyphlans and artiodactyls from the ratio shared by afrotherians, primates, scandentia and glires, and thus presumably also by ancestral mammals.
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Figure 10: Variation in the ratios between numbers of neurons in each structure and numbers of neurons in the rest of brain across clades show a relative increase in numbers of neurons in the cerebral cortex and cerebellum in both primates and artiodactyls. Each symbol represents the average values for the structures indicated in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). (A) Ratio between numbers of neurons in the cerebral cortex and rest of brain is higher in primates (13.58 ± 2.14, red) and artiodactyls (6.96 ± 1.11, pink) than in afrotherians (2.41 ± 0.18, blue), glires (2.11 ± 0.17, green), eulipotyphlans (2.04 ± 0.13, orange) and scandentia (2.69, gray). The arrows and the phylogenetic scheme on the left indicate the divergence of primates and artiodactyls from the ratio shared by afrotherians, eulipotyphlans, scandentia and glires, and thus presumably also by ancestral mammals. (B) Ratio between numbers of neurons in the cerebellum and rest of brain is also higher in primates (35.91 ± 6.95, red) and artiodactyls (37.34 ± 5.72, pink) than in afrotherians (6.88 ± 0.89, blue), glires (10.03 ± 1.05, green), eulipotyphlans (9.14 ± 2.05, orange) and scandentia (8.24, gray). The arrows and the phylogenetic scheme on the left indicate the divergence of primates and artiodactyls from the ratio shared by afrotherians, eulipotyphlans, scandentia and glires, and thus presumably also by ancestral mammals. (C) ratio between numbers of neurons in the olfactory bulb and rest of brain are larger than 1 only in eulipotyphlans (1.52 ± 0.31, orange), compared to 0.65 ± 0.11 in glires, 0.68 ± 0.22 in afrotherians, 0.49 ± 0.27 in primates, 0.56 in scandentia, and 0.23 ± 0.05 in artiodactyls. The arrows and the phylogenetic scheme on the left indicate the divergence of eulipotyphlans and artiodactyls from the ratio shared by afrotherians, primates, scandentia and glires, and thus presumably also by ancestral mammals.

Mentions: Afrotherians, glires, scandentia, and eulipotyphlans have on average 2.21 ± 0.22 neurons in the cerebral cortex to every neuron in the rest of brain, with ratios that are not significantly different across clades (ANOVA, p = 0.0783) and that do not vary in correlation with increasing numbers of neurons in the rest of brain (Spearman correlation, p > 0.5; Figure 10A). Thus, as the rest of brain gains neurons in these clades, the cerebral cortex does not gain relatively more neurons, maintaining a fairly stable ratio of approximately 2 neurons for every neuron in the rest of brain.


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)

Variation in the ratios between numbers of neurons in each structure and numbers of neurons in the rest of brain across clades show a relative increase in numbers of neurons in the cerebral cortex and cerebellum in both primates and artiodactyls. Each symbol represents the average values for the structures indicated in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). (A) Ratio between numbers of neurons in the cerebral cortex and rest of brain is higher in primates (13.58 ± 2.14, red) and artiodactyls (6.96 ± 1.11, pink) than in afrotherians (2.41 ± 0.18, blue), glires (2.11 ± 0.17, green), eulipotyphlans (2.04 ± 0.13, orange) and scandentia (2.69, gray). The arrows and the phylogenetic scheme on the left indicate the divergence of primates and artiodactyls from the ratio shared by afrotherians, eulipotyphlans, scandentia and glires, and thus presumably also by ancestral mammals. (B) Ratio between numbers of neurons in the cerebellum and rest of brain is also higher in primates (35.91 ± 6.95, red) and artiodactyls (37.34 ± 5.72, pink) than in afrotherians (6.88 ± 0.89, blue), glires (10.03 ± 1.05, green), eulipotyphlans (9.14 ± 2.05, orange) and scandentia (8.24, gray). The arrows and the phylogenetic scheme on the left indicate the divergence of primates and artiodactyls from the ratio shared by afrotherians, eulipotyphlans, scandentia and glires, and thus presumably also by ancestral mammals. (C) ratio between numbers of neurons in the olfactory bulb and rest of brain are larger than 1 only in eulipotyphlans (1.52 ± 0.31, orange), compared to 0.65 ± 0.11 in glires, 0.68 ± 0.22 in afrotherians, 0.49 ± 0.27 in primates, 0.56 in scandentia, and 0.23 ± 0.05 in artiodactyls. The arrows and the phylogenetic scheme on the left indicate the divergence of eulipotyphlans and artiodactyls from the ratio shared by afrotherians, primates, scandentia and glires, and thus presumably also by ancestral mammals.
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Figure 10: Variation in the ratios between numbers of neurons in each structure and numbers of neurons in the rest of brain across clades show a relative increase in numbers of neurons in the cerebral cortex and cerebellum in both primates and artiodactyls. Each symbol represents the average values for the structures indicated in one species (afrotherians, blue; glires, green; eulipotyphlans, orange; primates, red; scandentia, gray; artiodactyls, pink). (A) Ratio between numbers of neurons in the cerebral cortex and rest of brain is higher in primates (13.58 ± 2.14, red) and artiodactyls (6.96 ± 1.11, pink) than in afrotherians (2.41 ± 0.18, blue), glires (2.11 ± 0.17, green), eulipotyphlans (2.04 ± 0.13, orange) and scandentia (2.69, gray). The arrows and the phylogenetic scheme on the left indicate the divergence of primates and artiodactyls from the ratio shared by afrotherians, eulipotyphlans, scandentia and glires, and thus presumably also by ancestral mammals. (B) Ratio between numbers of neurons in the cerebellum and rest of brain is also higher in primates (35.91 ± 6.95, red) and artiodactyls (37.34 ± 5.72, pink) than in afrotherians (6.88 ± 0.89, blue), glires (10.03 ± 1.05, green), eulipotyphlans (9.14 ± 2.05, orange) and scandentia (8.24, gray). The arrows and the phylogenetic scheme on the left indicate the divergence of primates and artiodactyls from the ratio shared by afrotherians, eulipotyphlans, scandentia and glires, and thus presumably also by ancestral mammals. (C) ratio between numbers of neurons in the olfactory bulb and rest of brain are larger than 1 only in eulipotyphlans (1.52 ± 0.31, orange), compared to 0.65 ± 0.11 in glires, 0.68 ± 0.22 in afrotherians, 0.49 ± 0.27 in primates, 0.56 in scandentia, and 0.23 ± 0.05 in artiodactyls. The arrows and the phylogenetic scheme on the left indicate the divergence of eulipotyphlans and artiodactyls from the ratio shared by afrotherians, primates, scandentia and glires, and thus presumably also by ancestral mammals.
Mentions: Afrotherians, glires, scandentia, and eulipotyphlans have on average 2.21 ± 0.22 neurons in the cerebral cortex to every neuron in the rest of brain, with ratios that are not significantly different across clades (ANOVA, p = 0.0783) and that do not vary in correlation with increasing numbers of neurons in the rest of brain (Spearman correlation, p > 0.5; Figure 10A). Thus, as the rest of brain gains neurons in these clades, the cerebral cortex does not gain relatively more neurons, maintaining a fairly stable ratio of approximately 2 neurons for every neuron in the rest of brain.

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.