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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.
Barton,
Mosaic evolution of brain structure in mammals.
2000, Pubmed
Barton,
Mosaic evolution of brain structure in mammals.
2000,
Pubmed Breuker,
Functional evo-devo.
2006,
Pubmed Carroll,
Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution.
2008,
Pubmed Copp,
The genetic basis of mammalian neurulation.
2003,
Pubmed Desmond,
Internal luminal pressure during early chick embryonic brain growth: descriptive and empirical observations.
2005,
Pubmed Desmond,
Embryonic brain enlargement requires cerebrospinal fluid pressure.
1977,
Pubmed Dye,
Two independent spiral structures control cell shape in Caulobacter.
2005,
Pubmed Ettensohn,
Mechanisms of epithelial invagination.
1985,
Pubmed Fabian,
Calyculin A, an enhancer of myosin, speeds up anaphase chromosome movement.
2007,
Pubmed Filas,
Mechanical stress as a regulator of cytoskeletal contractility and nuclear shape in embryonic epithelia.
2011,
Pubmed Gato,
Why the embryo still matters: CSF and the neuroepithelium as interdependent regulators of embryonic brain growth, morphogenesis and histiogenesis.
2009,
Pubmed Gutzman,
Epithelial relaxation mediated by the myosin phosphatase regulator Mypt1 is required for brain ventricle lumen expansion and hindbrain morphogenesis.
2010,
Pubmed
,
Xenbase Gutzman,
Formation of the zebrafish midbrain-hindbrain boundary constriction requires laminin-dependent basal constriction.
2008,
Pubmed Hamburger,
A series of normal stages in the development of the chick embryo. 1951.
1992,
Pubmed Harrington,
Comparative analysis of neurulation: first impressions do not count.
2009,
Pubmed Hofman,
On the evolution and geometry of the brain in mammals.
1989,
Pubmed Hofmann,
Early developmental patterning sets the stage for brain evolution.
2010,
Pubmed Kinoshita,
Apical accumulation of Rho in the neural plate is important for neural plate cell shape change and neural tube formation.
2008,
Pubmed
,
Xenbase Koshiba-Takeuchi,
Reptilian heart development and the molecular basis of cardiac chamber evolution.
2009,
Pubmed Lee,
Studies on the mechanisms of neurulation in the chick: interrelationship of contractile proteins, microfilaments, and the shape of neuroepithelial cells.
1985,
Pubmed Lowery,
Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products.
2005,
Pubmed Lowery,
Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation.
2004,
Pubmed Lui,
Development and evolution of the human neocortex.
2011,
Pubmed Männer,
Correlation between the embryonic head flexures and cardiac development. An experimental study in chick embryos.
1993,
Pubmed Martin,
Pulsed contractions of an actin-myosin network drive apical constriction.
2009,
Pubmed Martin,
Pulsation and stabilization: contractile forces that underlie morphogenesis.
2010,
Pubmed McGowan,
Species differences in early patterning of the avian brain.
2011,
Pubmed Nelson,
Emergent patterns of growth controlled by multicellular form and mechanics.
2005,
Pubmed Nerurkar,
Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads.
2006,
Pubmed Northcutt,
Changing views of brain evolution.
2001,
Pubmed Nyholm,
A novel genetic mechanism regulates dorsolateral hinge-point formation during zebrafish cranial neurulation.
2009,
Pubmed Olson,
Gene regulatory networks in the evolution and development of the heart.
2006,
Pubmed Pincus,
Comparison of quantitative methods for cell-shape analysis.
2007,
Pubmed Raghavan,
Decoupling diffusional from dimensional control of signaling in 3D culture reveals a role for myosin in tubulogenesis.
2010,
Pubmed Rodriguez,
Stress-dependent finite growth in soft elastic tissues.
1994,
Pubmed Salazar-Ciudad,
A computational model of teeth and the developmental origins of morphological variation.
2010,
Pubmed Salazar-Ciudad,
Mechanisms of pattern formation in development and evolution.
2003,
Pubmed Schoenwolf,
Mechanisms of neurulation: traditional viewpoint and recent advances.
1990,
Pubmed Solon,
Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure.
2009,
Pubmed Sylvester,
Brain diversity evolves via differences in patterning.
2010,
Pubmed Taber,
Theoretical study of Beloussov's hyper-restoration hypothesis for mechanical regulation of morphogenesis.
2008,
Pubmed Voronov,
Cardiac looping in experimental conditions: effects of extraembryonic forces.
2002,
Pubmed Wozniak,
Mechanotransduction in development: a growing role for contractility.
2009,
Pubmed Xu,
Opening angles and material properties of the early embryonic chick brain.
2010,
Pubmed
