Altered developmental programs underlying the novel gut morphology of a cannibalistic anuran larva

Author(s): Ledon-Rettig CC, Womble M, Nascone-Yoder N

Summary:

The gut is a particularly fascinating organ from an ecological and evolutionary perspective; it dictates how well an organism digests and assimilates nutrients from its diet, and thus has a profound impact on fitness. Organisms vary widely in what they consume, and this dietary diversity is reflected by equally diverse variation in gut morphologies. For instance, anuran Xenopus laevis larvae maintain an elongate gut that is adaptive for their herbivorous diet (an ancestral condition). In contrast, larvae of Lepidobatrachus laevis are obligate carnivores (a derived condition) and possess a relatively short gut that is appropriate for their diet. Remarkably, little is known about how developmental programs have diverged to give rise to such variation in gut morphology. To reveal the developmental mechanisms underlying the evolution of the novel, short-gut morphology, we compared key features of gut morphogenesis between Xenopus and Lepidobatrachus. In Xenopus, all endodermal cells of the primitive gut tube become polarized, undergo radial intercalation and contribute to gut elongation as they become incorporated into the gut epithelium. In contrast, in Lepidobatrachus, many central endodermal cells do not undergo radial intercalation and therefore cannot contribute to elongation. Additionally, many cells in the developing epithelium of Lepidobatrachus undergo programmed cell death and are extruded, further limiting the endodermal contribution to elongation. This programmed cell death – which typically occurs during thyroid hormone-dependent metamorphosis in Xenopus – is correlated with the expression of thyroid hormone signaling components in Lepidobatrachus, suggesting that precocious thyroid hormone signaling in the developing intestine is, in part, responsible for their novel gut topology.