Mapping behavioural evolution onto brain evolution: the strategic roles of conserved organization in individuals and species

Abstract

The pattern of individual variation in brain component structure in pigs, minks and laboratory mice is very similar to variation across species in the same components, at a reduced scale. This conserved pattern of allometric scaling resembles robotic architectures designed to be robust to changes in computing power and task demands, and may reflect the mechanism by which both growing and evolving brains defend basic sensory, motor and homeostatic functions at multiple scales. Conserved scaling rules also have implications for species-specific sensory and social communication systems, motor competencies and cognitive abilities. The role of relative changes in neuron number in the central nervous system in producing species-specific behaviour is thus highly constrained, while changes in the sensory and motor periphery, and in motivational and attentional systems increase in probability as the principal loci producing important changes in functional neuroanatomy between species. By their nature, these loci require renewed attention to development and life history in the initial organization and production of species-specific behavioural abilities.

Figure 1.

In all graphs, the percentage variance in each structure described by the first principal component (PC1) is graphed by the black bars, and the second principal component (PC2) by the white bars, the total percentage variance differing in each case. (a) ‘Phylogenetic variability’, based on a sample of 131 species of bats, primates and insectivores. PC1 accounts in total for 96.47 and PC2, 2.61%. (b) ‘Individual variability, Composite’ includes 47 individuals whose scores were entered as deviations from cell means so as to exclude species and sex differences, where the cells were six male wild mink, six female wild mink, six male domestic mink, six female domestic mink, six wild pigs of unknown sex, six domestic pigs of unknown sex and 11 mouse strains. PC1 accounts for 72.48% of the variance, and PC2 for 7.9%. For the individual species, (c) pig, (d) mink and (e) mouse, data are plotted so that their overall pattern might be examined, but no statistical claims about factor loadings on individual structures are made at the individual species level.

Figure 2.

Values of PC1 and PC2, expressed as a z-score for each individual animal for the population of 47 individuals. Three of the mice and one pig fall outside the 90% delimiter (dashed line); these mouse strains are WSB/ei, MOLC/ei and MOLf/ei. Mouse strains may be intrinsically more variable because of greater genetic difference than the minks and pigs, whose lineages are unknown, but whatever the cause, their deviation from the phylogenetic and the other individuals is pronounced. Diamonds, minks; open circles, pigs; filled circles, mice.

Figure 3.

Comparison of the ratio of cortex to total brain volume in seven wild/domestic comparisons gathered by Kruska, compared with equal proportionality (dashed line) or to cortex hyperallometry determined phylogenetically (solid line). In five of the seven comparisons, cortex volume is reduced more than overall brain volume.