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. 2013 Jun 26:7:16.
doi: 10.3389/fnana.2013.00016. eCollection 2013.

The secondary loss of gyrencephaly as an example of evolutionary phenotypical reversal

Iva Kelava  1 , Eric Lewitus, Wieland B Huttner
Affiliations

The secondary loss of gyrencephaly as an example of evolutionary phenotypical reversal

Iva Kelava et al. Front Neuroanat. .

Abstract

Gyrencephaly (the folding of the surface of the neocortex) is a mammalian-specific trait present in almost all mammalian orders. Despite the widespread appearance of the trait, little is known about the mechanism of its genesis or its adaptive significance. Still, most of the hypotheses proposed concentrated on the pattern of connectivity of mature neurons as main components of gyri formation. Recent work on embryonic neurogenesis in several species of mammals revealed different progenitor and stem cells and their neurogenic potential as having important roles in the process of gyrification. Studies in the field of comparative neurogenesis revealed that gyrencephaly is an evolutionarily labile trait, and that some species underwent a secondary loss of a convoluted brain surface and thus reverted to a more ancient form, a less folded brain surface (lissencephaly). This phenotypic reversion provides an excellent system for understanding the phenomenon of secondary loss. In this review, we will outline the theory behind secondary loss and, as specific examples, present species that have undergone this transition with respect to neocortical folding. We will also discuss different possible pathways for obtaining (or losing) gyri. Finally, we will explore the potential adaptive consequence of gyrencephaly relative to lissencephaly and vice versa.

Keywords: brain evolution; gyrencephaly; lissencephaly; neocortex; reverse evolution.

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Figures

Figure 1
Figure 1
Gyrencephalic brains. (A) Brains of the lion (top) and the house cat (bottom). Despite a different level of gyrification, note the similarities in the pattern of gyri and sulci distribution. After Welker (1990). Homologous gyri are colored to facilitate comparison. (B) A coronal section of the human brain showing gryi and sulci. This image does not follow the scale bar in (A).
Figure 2
Figure 2
Theories of gyrogenesis. (A) Neuronal tension (Van Essen, ; Mota and Herculano-Houzel, 2012). This theory stresses the differential pulling forces of the underlying white matter on the neocortex, resulting in the convoluted appearance of the brain. (B) Differential growth (Richman et al., ; Kriegstein et al., 2006) theory states that the folding of the neocortex is a result of the differential expansion of uppers versus lower neuronal layers. (C) Welker (1990) emphasizes various processes involved in gryogenesis, including the orientation of neurons, their arborization and incoming fibers. See main text.
Figure 3
Figure 3
Examples of potentially secondarily lissencephalic brains. (A) Top left: Common marmoset, middle left: rat, bottom left: mouse. Right: West Indian manatee. (B) Brains of three extant mustelid species. Note the simplification of the gyrification pattern in smaller brains. The gyri in smaller brains are also shallower. Below is the phylogenetic tree [after Koepfli et al. (2008)] showing the relationships between these species and their time of divergence.
Figure 4
Figure 4
Neurogenic program is a limiting factor on GI potential. A cartoon illustrating the concept that the range of GI achievable is determined by the cell-biological features of a species neurogenic program. For example, species without proliferative progenitor-types in the basal compartment may be limited to GIs below a certain value (dotted vertical line), whereas species with such a progenitor-type are only constrained by a lower GI limit. Note that if a range of GI values may be achieved without adapting cell-biological features of the neurogenic period, then species in the lower GI range are likely to show frequent evolutionary increases and decreases in GI.
Figure 5
Figure 5
Evolution of the neocortex. Lineages leading to extant species. (A) Increase in brain size led to the increase in GI. The processes leading to this transition might have been that the bRG were present at a certain significant number (marked by green letters) and that they have evolved the ability to produce TAPs. Example: human. (B) Dwarfing I. Decrease in brain and body size relative to the ancestor is accompanied by a reduction in GI. The reduction in the number of bRG might have underlain this transition. Examples: mouse and beaver. (C) Dwarfing II. A similar process as in (B), but the lissencephaly is due to changes in cell-biological parameters of progenitor cells (e.g., cell cycle), not their numbers. Example: marmoset. (D) Increase in brain and body size is accompanied by a decrease in GI. Example: manatee. Images for the ancestor and the transitional form are for illustration purposes only. Images drawn from photos obtained from www.brainmuseum.org and are not to scale.
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