Cortical evolution in mammals: the bane and beauty of phenotypic variability

Abstract

Evolution by natural selection, the unifying theory of all biological sciences, provides a basis for understanding how phenotypic variability is generated at all levels of organization from genes to behavior. However, it is important to distinguish what is the target of selection vs. what is transmitted across generations. Physical traits, behaviors, and the extended phenotype are all selected features of an individual, but genes that covary with different aspects of the targets of selection are inherited. Here we review the variability in cortical organization, morphology, and behavior that have been observed across species and describe similar types of variability within species. We examine sources of variability and the constraints that limit the types of changes that evolution has and can produce. Finally, we underscore the importance of how genes and genetic regulatory networks are deployed and interact within an individual, and their relationship to external, physical forces within the environment that shape the ultimate phenotype.

Fig. 1.

Cladogram of phylogenetic relationships for the major subclasses of mammals. All species examined have a constellation of cortical fields that includes primary somatosensory, visual, and auditory areas (see color codes). However, their relative size and location has been altered in different species.

Fig. 2.

Schematic of the types of cross-species, systems-level modifications that have been observed in the neocortex. The outline of the boxes indicates the entire cortical sheet, and smaller boxes within represent either cortical domains (B), cortical fields (C and E–G), or representations within cortical fields (D). These same types of changes have been observed across individuals within a species, but they are often less dramatic.

Fig. 3.

Examples of cortical magnification for (A) the bill of the platypus, (B) the nose tentacles of the star-nosed mole, (C) the hand of the raccoon, and (D) the whiskers of the rat. The representation of the specialized morphological structures in S1 is red and in other cortical areas is pink. Gray indicates the representation of the rest of the body in S1.

Fig. 4.

(A) Wing of a bat, (B) pectoral fin of a dolphin, and (C) hand of a human are examples of homologous morphological structures. Although they are used for very different purposes, they are organized around the same basic skeletal frame (in gray).

Fig. 6.

Graded patterns of expression of transcription factors (Upper) involved in aspects of arealization such as location and size of cortical fields. Knockout (KO; Lower) of these transcription factors generates radically different sizes and positions of cortical fields compared with wild-type mice (Left). Cortical fields are color-coded (see key at bottom). Adapted from ref. .

Fig. 5.

Examples of intraspecies variability for (A) motor cortex in mice (adapted from ref. 41), (B) area 5 in macaque monkeys (adapted from ref. 24), (C) ocular dominance columns in squirrel monkeys (adapted from ref. 47), (D) S1 architectonic isomorphs in the owl monkey face representation (adapted from ref. 45), and (E) hand representation (adapted from ref. 46). In mice, motor maps are grossly topographically organized but are locally fractured. A depicts motor maps from two different individual mice. Each small square represents a microstimulation location that evoked a movement of a particular body part, color-coded according to the colored mouse body at top. In macaques (B), maps of posterior parietal area 5 are highly variable and are fractured. Area 5 also demonstrates an extreme magnification of the forelimb. Color codes of the hand and arm correspond to their representations in cortical maps. In squirrel monkeys (C) ocular dominance columns vary from highly distinct (leftmost square) to nonexistent (far right square). Finally, the myeloarchitectonically distinct modules of the face (D) and hand (E) representations in S1 of owl monkeys vary in their specific size and shape between individual animals. Color codes of the hand and face correspond to their representations in cortical maps.

Fig. 7.

Schematic illustration demonstrating how covaration between the targets of selection, phenotypic organization, and genetic events could lead to inheritance of genes that generate a population of future individuals with a unique combination of phenotypic characteristics. Blue shading corresponds to factors associated with forelimb morphology, and green shading corresponds to factors associated with brain organization. These are not mutually exclusive but interact to some extent (overlapped shading). The Gaussian curves represent the range of naturally occurring variability in a specific characteristic, with narrower curves representing robust characteristics and wider curves representing stochastic characteristics. The black and gray circles represent the location of the optimal characteristic along the current distribution (solid curve). Selection pressures will eventually push the population to a new distribution, centered around the optimal characteristic (dashed curve). In this example our species is an echolocating bat, and our environmental context is illustrated at the top. Some of the targets of selection (Gaussian curves inside the red, dashed oval) would be characteristics of the forelimb that allow for flight, as well as behaviors such as fast response time and good auditory discrimination. Cortical phenotypic characteristics (located between the dark gray and red dashed lines) that underlie auditory and tactile discriminatory ability would include an increase in the size of S1 and A1, as well as an increase in the wing representation within S1. Underlying developmental processes associated with wing formation include a decrease in apoptosis in the interdigit membrane and the growth of the limb. At the far perimeter (far left and far right) of this illustration are the genetic events that covary with aspects of the body and brain phenotypes.