title: Heterochrony and early left-right asymmetry in the development of the cardiorespiratory system of snakes.
abstract: Snake lungs show a remarkable diversity of organ asymmetries. The right lung is always fully developed, while the left lung is either absent, vestigial, or well-developed (but smaller than the right). A 'tracheal lung' is present in some taxa. These asymmetries are reflected in the pulmonary arteries. Lung asymmetry is known to appear at early stages of development in Thamnophis radix and Natrix natrix. Unfortunately, there is no developmental data on snakes with a well-developed or absent left lung. We examine the adult and developmental morphology of the lung and pulmonary arteries in the snakes Python curtus breitensteini, Pantherophis guttata guttata, Elaphe obsoleta spiloides, Calloselasma rhodostoma and Causus rhombeatus using gross dissection, MicroCT scanning and 3D reconstruction. We find that the right and tracheal lung develop similarly in these species. By contrast, the left lung either: (1) fails to develop; (2) elongates more slowly and aborts early without (2a) or with (2b) subsequent development of faveoli; (3) or develops normally. A right pulmonary artery always develops, but the left develops only if the left lung develops. No pulmonary artery develops in relation to the tracheal lung. We conclude that heterochrony in lung bud development contributes to lung asymmetry in several snake taxa. Secondly, the development of the pulmonary arteries is asymmetric at early stages, possibly because the splanchnic plexus fails to develop when the left lung is reduced. Finally, some changes in the topography of the pulmonary arteries are consequent on ontogenetic displacement of the heart down the body. Our findings show that the left-right asymmetry in the cardiorespiratory system of snakes is expressed early in development and may become phenotypically expressed through heterochronic shifts in growth, and changes in axial relations of organs and vessels. We propose a step-wise model for reduction of the left lung during snake evolution.
authors.affiliation: Institute of Biology, University of Leiden, Leiden, the Netherlands.
authors.forename: Benjamin J
authors.initials: BJ
authors.lastname: van Soldt
authors.affiliation: Department of Theoretical Biology, University of Vienna, Vienna, Austria.
authors.forename: Brian D
authors.initials: BD
authors.lastname: Metscher
authors.affiliation: Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, the Netherlands.
authors.forename: Robert E
authors.initials: RE
authors.lastname: Poelmann
authors.affiliation: Department of Biology, University of Antwerp, Antwerp, Belgium.
authors.forename: Bart
authors.initials: B
authors.lastname: Vervust
authors.affiliation: Institute of Biology, University of Leiden, Leiden, the Netherlands; NCB Naturalis, Leiden, the Netherlands.
authors.forename: Freek J
authors.initials: FJ
authors.lastname: Vonk
authors.affiliation: Department of Theoretical Biology, University of Vienna, Vienna, Austria.
authors.forename: Gerd B
authors.initials: GB
authors.lastname: Müller
authors.affiliation: Institute of Biology, University of Leiden, Leiden, the Netherlands.
authors.forename: Michael K
authors.initials: MK
authors.lastname: Richardson
mesh_terms: D000818:Animals; D019521:Body Patterning; D002319:Cardiovascular System / Q000033:anatomy & histology* / Q000196:embryology / Q000254:growth & development; D006321:Heart / Q000033:anatomy & histology / Q000196:embryology; D021621:Imaging, Three-Dimensional; D008168:Lung / Q000098:blood supply* / Q000196:embryology / Q000254:growth & development; D008953:Models, Anatomic; D010802:Phylogeny; D011651:Pulmonary Artery / Q000033:anatomy & histology* / Q000196:embryology / Q000254:growth & development; D012137:Respiratory System / Q000033:anatomy & histology* / Q000196:embryology / Q000254:growth & development; D012911:Snakes / Q000145:classification / Q000196:embryology / Q000235:genetics; D013045:Species Specificity; D055114:X-Ray Microtomography / Q000379:methods