Elsevier

Tissue and Cell

Volume 35, Issue 5, October 2003, Pages 375-391
Tissue and Cell

A systematic study of the development of the airway (bronchial) system of the avian lung from days 3 to 26 of embryogenesis: a transmission electron microscopic study on the domestic fowl, Gallus gallus variant domesticus

https://doi.org/10.1016/S0040-8166(03)00058-2Get rights and content

Abstract

In the embryo of the domestic fowl, Gallus gallus variant domesticus, the lung buds become evident on day 3 of development. After fusing on the ventral midline, the single entity divides into left and right primordial lungs that elongate caudally while diverging and shifting towards the dorsolateral aspects of the coelomic cavity. On reaching their definitive topographical locations, the lungs rotate along a longitudinal axis, attach, and begin to slide into the ribs. First appearing as a solid cord of epithelial cells that runs in the proximal-distal axis of the developing lung, progressively, the intrapulmonary primary bronchus begins to canalize. In quick succession, secondary bronchi sprout from it in a craniocaudal sequence and radiate outwards. On reaching the periphery of the lung, parabronchi (tertiary bronchi) bud from the secondary bronchi and project into the surrounding mesenchymal cell mass. The parabronchi canalize, lengthen, increase in diameter, anastomose, and ultimately connect the secondary bronchi. The luminal aspect of the formative parabronchi is initially lined by a composite epithelium of which the peripheral cells attach onto the basement membrane while the apical ones project prominently into the lumen. The epithelium transforms to a simple columnar type in which the cells connect through arm-like extensions and prominently large intercellular spaces form. The atria are conspicuous on day 15, the infundibulae on day 16, and air capillaries on day 18. At hatching (day 21), the air and blood capillaries have anastomosed profusely and the blood–gas barrier become remarkably thin. The lung is well developed and potentially functionally competent at the end of the embryonic life. Thereafter, at least upto day 26, no further consequential structures form. The mechanisms by which the airways in the avian lung develop fundamentally differ from those that occur in the mammalian one. Compared with the blind-ended bronchial system that inaugurates in the mammalian lung, an elaborate, continuous system of air conduits develops in the avian one. Further studies are necessary to underpin the specific molecular factors and genetic processes that direct the morphogenesis of an exceptionally complex and efficient respiratory organ.

Introduction

Albeit having been continually studied for well over the last four centuries, e.g. since Coitier (1573), certain fundamental aspects of the structure and function of the avian respiratory system are still ambiguous (e.g. Scheid, 1990, Maina, 2002a). While on account of birds and mammals being immediate vertebrate taxa that along the evolutionary continuum split at different times from a common reptilian (cotylosaurian) stock (e.g. Pough et al., 1989) shared morphological features would be expected, regarding the respiratory systems, the avian (parabronchial) lung differs in certain quintessential ways from the reptilian (faveolar), and the mammalian (bronchioalveolar) ones (e.g. Duncker, 1978a, Weibel, 1984, Maina et al., 1989a, Maina et al., 1999, Maina, 1990, Maina, 2002a). The avian respiratory system, the lung air-sac system, evinces exceptional structural complexity (e.g. Duncker, 1974, Duncker, 1978a, King and McLelland, 1989; Maina, 1996, Maina, 1998, Maina, 2002a, Maina, 2002b, Maina, 2002c) and remarkable functional efficiency (e.g. Scheid, 1979, Fedde, 1980, Seller, 1987, King and McLelland, 1989). While the arrangement of the bronchial (airway) system of the mammalian lung displays iterating, commonly dichotomous bifurcation that terminates in blind-ended air conduits that fashion the so-called “respiratory tree” (e.g. Horsfield, 1997, Maina and van Gils, 2001), in the avian lung, a highly intricate, anastomotic system exists. Regarding the architecture of the avian lung, Campana (1875), Locy and Larsell (1916a), and Bellairs and Osmond (1998), respectively remarked that in the avian lung “there is no bronchial tree in the sense in which this designation is used for mammals”; “the establishment of labrinthine communications between all parts of the bronchial tree imparts to the avian lung a unique architecture not found in other classes of vertebrates”; and that “a system of airways that resembles a sponge in structure” exists.

While the morphological and morphometric attributes of the mature avian respiratory system are now reasonably well understood (e.g. Duncker, 1974, Dubach, 1981, Duncker and Guntert, 1985, Maina, 1989, Maina, 2002a, Maina et al., 1989b) and the plausible modalities of the evolution of the parabronchial lung from the faveolar one have been well expressed (e.g. Perry, 1989, Perry, 1992, Perry, 1999), little is, however, known about the specific spatial-temporal dynamics of the mechanisms by which the exceptionally complex structure, and the remarkable functional competency of the lung air-sac system are morphogenetically engineered. Nearly a century ago, Locy and Larsell (1916b, p. 35) predictably pointed out that “the morphology of the avian lung can be made clear only by observations of its development, and it is through this channel alone that one becomes acquainted with the nature of the modifications of the bird’s lung that place it in a class by itself.” Such pedagogic actuality notwithstanding, compared with the mammalian lung of which the early development is now well known (for reviews see, e.g. Burri and Weibel, 1977, Adamson, 1997, Hislop, 2002), relatively little work has been done on the avian respiratory system where on the whole comprehensive studies are lacking. Investigations like those by Selenka (1866), Juillet (1912), Larsell (1914), Locy and Larsell, 1916a, Locy and Larsell, 1916b, Delphia (1958), Petrik (1967), Petrik and Riedel (1968), Jones and Radnor, 1972a, Jones and Radnor, 1972b, Duncker (1978b), and Gallanger (1986) lack explicative morphogenetic details regarding the dynamics of the fabrication of many structural components. Of particular concern is the fact that between the studies where characterization of the development of the avian respiratory system has been attempted, significant discrepancies exist. Even in the domestic fowl, Gallus gallus variant domesticus, the only bird that has been meaningfully investigated, inconsistencies on chronological staging, and observations on morphogenetic transformations and topographical translocations preponderate (e.g. Locy and Larsell, 1916a, Locy and Larsell, 1916b; Duncker, 1978b, Bellairs and Osmond, 1998). De facto, the state of the existing knowledge on the development of the avian respiratory system is both inadequate and irreconcilable in many ways. Locy and Larsell’s works (Locy and Larsell, 1916a, Locy and Larsell, 1916b) on the domestic fowl that were performed entirely by light microscopy and airway and vascular injections, perceptibly owing to the then existing methodological limitations and technological strictures, are ostensibly the only particularly noteworthy systematic studies that cover the entire embryonic period of the growth and development of the avian respiratory system in meaningful depth. Still, as the investigators themselves point out (Locy and Larsell, 1916a, p. 449), the studies were neither fully comprehensive nor were they entirely conclusive.

After having been relegated to the background since between the 1920s and 1930s with the advent of what was termed “Modern Synthesis” (e.g. Morgan, 1932, Morgan, 1934), i.e. the integration of population genetics with evolutionary biology, developmental biology (embryology) has now unquestionably reclaimed its befitting place as an integral investigative approach for understanding and explicating the mechanisms and processes that accompany evolutionary and adaptive change, especially in complex biological systems (e.g. Atchley and Hall, 1991, Dassow and Munro, 1999). Synthesis of evolutionary and developmental biology, now dubbed EvoDevo (e.g. Gilbert et al., 1996), is an inclusive, highly powerful method of elucidating morphological and functional novelty (e.g. Patel, 1994, Sommer and Sternberg, 1996, Valentine et al., 1996). The import of the multidisciplinary integration was remarked on by Gilbert et al. (1996) as follows: “to go from functional biology to evolutionary biology without considering developmental biology is like going from displacement to acceleration without considering velocity.” It is inherently impotent to practically or conceptually endeavor to meaningfully progress from one level of biological understanding to the other without considering the modalities of the fabrication of the structural components, the constitutive elements that grant the essential templates for evolutionary and adaptive change. Dearth of detailed, extensive data on the morphogenesis of the avian respiratory system has unquestionably hindered decisive perception of its functional design. This investigation is a part of a continuing, multifaceted effort striving to provide details on the timing and consecution of the developmental events and processes that prescribe, direct, and produce an exceptionally elaborate and functionally competent respiratory organ. On the whole, birds grant an ideal organismal paradigm for understanding the morphological and physiological requisites for evolution, adaptation, and advancement to high metabolic states.

Section snippets

Materials and methods

Fertile eggs of the New Hampshire breed of chicken, Gallus gallus variant domesticus were acquired from a commercial breeder through the Central Animal Services of the University of the Witwatersrand (Animal Ethics Clearance No.: 2001/82/1). Freshly laid eggs were used. They came from same crutches and were of fairly the same size. The eggs were incubated under a thermostatically regulated temperature of 37.5 °C, 21% oxygen, and humidity maintained by a constant reservoir of water. The eggs were

Results

The developing lung buds were first perceptible on day 3 of embryogenensis. They appeared as paired protuberances on the lateroventral aspect of the foregut (primitive pharynx) of the developing embryo. The buds (Fig. 1) approached each other on the ventral midline and fused. On day 5, the single bud divided into rather sacccular primordial left and a right lungs that progressively extended caudally while separating and shifting towards the opposite dorsolateral aspects of the body wall. The

Discussion

In biology, regarding aspects of structure and function, notwithstanding immense commitment of investigative effort, few organs have ostensibly remained as poorly understood as the avian respiratory system, the lung air-sac system. Farner (1970) observed that “historically, the avian respiratory system is highly ranked among the controversial organ-systems” while Duncker (1974) remarked that “the avian respiratory tract has been investigated by scientists as long as they have been studying

Acknowledgements

This study was funded by a University of the Witwatersrand Research Council grant. I wish to thank Ms. G. Veale, A. Mortimer, and P. Sharp for technical assistance and Mr. P. Dawson and L. Sinclair for logistical assistance with the procurement of the eggs. This paper was prepared while on a sabbatical leave at the Department of Medicine (Physiology Section) of the University of California, San Diego. I wish to thank Prof. J.B. West for hosting me in his laboratory and the National Institutes

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