Fluid dynamics in developmental biology: moving fluids that shape ontogeny

Abstract

Human conception, indeed fertilization in general, takes place in a fluid, but what role does fluid dynamics have during the subsequent development of an organism? It is becoming increasingly clear that the number of genes in the genome of a typical organism is not sufficient to specify the minutiae of all features of its ontogeny. Instead, genetics often acts as a choreographer, guiding development but leaving some aspects to be controlled by physical and chemical means. Fluids are ubiquitous in biological systems, so it is not surprising that fluid dynamics should play an important role in the physical and chemical processes shaping ontogeny. However, only in a few cases have the strands been teased apart to see exactly how fluid forces operate to guide development. Here, we review instances in which the hand of fluid dynamics in developmental biology is acknowledged, both in human development and within a wider biological context, together with some in which fluid dynamics is notable but whose workings have yet to be understood, and we provide a fluid dynamicist's perspective on possible avenues for future research.

Figure 1. Role of cytoplasmic streaming in cellular growth.

(i) Proximal streaming in the wild-type C. elegans gonad and its role in oocyte growth. (A) Diagram of one arm of an adult hermaphrodite gonad. Plasma membranes, red; nuclei, blue. Somatic sheath cells enclose most of the gonad, but are not shown for simplicity. (B) Single image from time-lapse movie. DIC particles are shown at high magnification in inset. (C) 2-min particle tracks. (Wolke et al., 2007). (ii) Spiral rotational streaming in Chara corallina internodal cell. Regions of opposite flow direction are arranged like the colors on a barber pole, separated by two spiraling lines of missing chloroplasts termed indifferent zones. (i) is reproduced with the permission of the Company of Biologists.

Figure 2. Fluid flow in the development of the body plan.

(i) Polarity establishment in C. elegans. Anterior is at the left. Some component of the asters of the sperm pronucleus induces relaxation of cortical tension at the posterior end of the egg (A). This induces a movement of contractile elements from this end [curved arrows in (B)], and a simultaneous flow of cytoplasm towards this [straight arrow in (B)]. (C) P granules (black circles) are segregated to the posterior end of the egg by the cytoplasmic flow. (ii) Left-right development in vertebrates. Node of the mouse embryo (a) and leftward transport of microbeads by the cilia induced nodal flow (b). (i) © Hird and White, 1993. Originally published in (Hird, 1993). (ii) (A) (from Vogan and Tabin, 1999) and (B) (from Nonaka et al., 2002) are reprinted by permission of Macmillan Publishers, Ltd.

Figure 3. Fluid flow implicated in organogenesis in mouse (A)–(C), zebrafish (D)–(J) and fruit fly (K)–(L) embryos.

(A)–(B) Flow of aqueous humour: first produced in the ciliary body of the eye, it circulates throughout the anterior part of the eye, and then exits primarily through the trabecular meshwork (Calera et al., 2006; Alward, 2003). (C) Flow of exogenously microinjected India ink in the mouse brain showing the direction of the cerebrospinal flow and the parallel neuroblast migration (Sawamoto et al., 2006). (D) Fluid flow in the central canal of the spinal cord in a zebrafish embryo (Kramer-Zucker et al., 2005). (E)–(F) Beating cilia and kinocilia in zebrafish ear during otolith seeding (Hammond and Whitfield, 2006; Riley et al., 1997). (G)–(H) Cilia in the pronephric ducts (arrows indicate the point were the pronephric ducts merge at the cloaca) and the associated flow through the pronephric kidney observed by injected dye into the circulation (Kramer-Zucker et al., 2005). (I)–(J) Valveless atrio-ventricular junction in the embryonic zebrafish heart indicating mean flow direction (red arrows) and streak-like imprints left by moving blood cells (Hove et al., 2003). (K)–(L) Liquid clearance and gas filling of a Drosophila embryo. The initiation of the gas filling (first gas bubble) and its completion, when all tracheal branches are gas filled, are shown (Tsarouhas et al., 2007). (A), (D), (E), (G) and (H) are reproduced with the permission of the Company of Biologists. (B) from Alward, 2003 and (C) from Sawamoto et al., 2006 are reprinted with permission of AAAS. (F) from Riley et al., 1997, (K) and (L) from Tsarouhas et al., 2007 are reprinted with permission of Elsevier. (I) and (J) are reprinted by permission of Macmillan Publishers, Ltd. (Hove et al., 2003).

Figure 4. Phenotypical response of a sessile organism to flow: Growth forms of the stony coral

Form (A) originates from an exposed site, (B) from a semiprotected site, and (C) from a site sheltered from water movement. Reprinted by permission of the American Physical Society (Kaandorp et al., 1996).

Figure 5. Flow regulation in the extraembryonic fluid: time-lapse video micrographs of the pond snail Helisoma trivolvis embryo showing embryo spinning within the egg.

Arrowheads in the first, fifth, sixth, and tenth frames of the image series reference the angular change in position of the foot primordium. The diagonal band in the lower left corner of each frame is the egg capsule wall (Diefenbach et al., 1991). Reprinted by permission of Wiley & Sons, Ltd.