title: A potential role for differential contractility in early brain development and evolution.
abstract: Differences in brain structure between species have long fascinated evolutionary biologists. Understanding how these differences arise requires knowing how they are generated in the embryo. Growing evidence in the field of evolutionary developmental biology (evo-devo) suggests that morphological differences between species result largely from changes in the spatiotemporal regulation of gene expression during development. Corresponding changes in functional cellular behaviors (morphogenetic mechanisms) are only beginning to be explored, however. Here we show that spatiotemporal patterns of tissue contractility are sufficient to explain differences in morphology of the early embryonic brain between disparate species. We found that enhancing cytoskeletal contraction in the embryonic chick brain with calyculin A alters the distribution of contractile proteins on the apical side of the neuroepithelium and changes relatively round cross-sections of the tubular brain into shapes resembling triangles, diamonds, and narrow slits. These perturbed shapes, as well as overall brain morphology, are remarkably similar to those of corresponding sections normally found in species such as zebrafish and Xenopus laevis (frog). Tissue staining revealed relatively strong concentration of F-actin at vertices of hyper-contracted cross-sections, and a finite element model shows that local contraction in these regions can convert circular sections into the observed shapes. Another model suggests that these variations in contractility depend on the initial geometry of the brain tube, as localized contraction may be needed to open the initially closed lumen in normal zebrafish and Xenopus brains, whereas this contractile machinery is not necessary in chick brains, which are already open when first created. We conclude that interspecies differences in cytoskeletal contraction may play a larger role in generating differences in morphology, and at much earlier developmental stages, in the brain than previously appreciated. This study is a step toward uncovering the underlying morphomechanical mechanisms that regulate how neural phenotypic differences arise between species.
authors.affiliation: Department of Biomedical Engineering, Washington University, One Brookings Drive, Campus Box 1097, Saint Louis, MO 63130-4899, USA.
authors.forename: Benjamen A
authors.initials: BA
authors.lastname: Filas
authors.forename: Alina
authors.initials: A
authors.lastname: Oltean
authors.forename: David C
authors.initials: DC
authors.lastname: Beebe
authors.forename: Ruth J
authors.initials: RJ
authors.lastname: Okamoto
authors.forename: Philip V
authors.initials: PV
authors.lastname: Bayly
authors.forename: Larry A
authors.initials: LA
authors.lastname: Taber
mesh_terms: D000818:Animals; D005075:Biological Evolution; D001921:Brain / Q000196:embryology* / Q000254:growth & development*; D002645:Chickens; D055119:Elastic Modulus / Q000502:physiology; D047108:Embryonic Development / Q000502:physiology*; D018507:Gene Expression Regulation, Developmental / Q000502:physiology*; D006801:Humans; D040542:Mechanotransduction, Cellular / Q000502:physiology*; D008959:Models, Neurological; D013045:Species Specificity; D014982:Xenopus laevis; D015027:Zebrafish