The Presence of a Functionally Tripartite Through-Gut in Ctenophora Has Implications for Metazoan Character Trait Evolution

• Published in: Current biology 2016-10, Vol.26 (20), p.2814-2820
• Main Authors: Presnell, Jason S., Vandepas, Lauren E., Warren, Kaitlyn J., Swalla, Billie J., Amemiya, Chris T., Browne, William E.
• Format: Article
• Language: English
• Subjects: alimentary canal; Animals; anus; Biological Evolution; Ctenophora; Ctenophora - anatomy & histology; Ctenophora - physiology; ctenophore; evolution; Gastrointestinal Tract - anatomy & histology; Gastrointestinal Tract - physiology; metazoan; non-bilaterian; through-gut
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2016.08.019

The current paradigm of gut evolution assumes that non-bilaterian metazoan lineages either lack a gut (Porifera and Placozoa) or have a sac-like gut (Ctenophora and Cnidaria) and that a through-gut originated within Bilateria [1–8]. An important group for understanding early metazoan evolution is Ctenophora (comb jellies), which diverged very early from the animal stem lineage [9–13]. The perception that ctenophores possess a sac-like blind gut with only one major opening remains a commonly held misconception [4, 5, 7, 14, 15]. Despite descriptions of the ctenophore digestive system dating to Agassiz [16] that identify two openings of the digestive system opposite of the mouth—called “excretory pores” by Chun [17], referred to as an “anus” by Main [18], and coined “anal pores” by Hyman [19]—contradictory reports, particularly prominent in recent literature, posit that waste products are primarily expelled via the mouth [4, 5, 7, 14, 19–23]. Here we demonstrate that ctenophores possess a unidirectional, functionally tripartite through-gut and provide an updated interpretation for the evolution of the metazoan through-gut. Our results resolve lingering questions regarding the functional anatomy of the ctenophore gut and long-standing misconceptions about waste removal in ctenophores. Moreover, our results present an intriguing evolutionary quandary that stands in stark contrast to the current paradigm of gut evolution: either (1) the through-gut has its origins very early in the metazoan stem lineage or (2) the ctenophore lineage has converged on an arrangement of organs functionally similar to the bilaterian through-gut. [Display omitted] •The Ctenophora, a non-bilaterian animal lineage, possess a functional though-gut•Evacuation of waste material via anal pores is controlled by actin-rich sphincters•We describe gut cell types involved with nutrient absorption and distribution•Homology of the ctenophore through-gut to the bilaterian through-gut remains unclear Ctenophores have historically been described as having a blind, sac-like gut. Using live imaging of ctenophore digestion in their report, Presnell et al. demonstrate that ctenophores possess a functionally tripartite through-gut, challenging the current paradigm that assumes that the through-gut originated within Bilateria.