title: Recurrent gene loss correlates with the evolution of stomach phenotypes in gnathostome history.
abstract: The stomach, a hallmark of gnathostome evolution, represents a unique anatomical innovation characterized by the presence of acid- and pepsin-secreting glands. However, the occurrence of these glands in gnathostome species is not universal; in the nineteenth century the French zoologist Cuvier first noted that some teleosts lacked a stomach. Strikingly, Holocephali (chimaeras), dipnoids (lungfish) and monotremes (egg-laying mammals) also lack acid secretion and a gastric cellular phenotype. Here, we test the hypothesis that loss of the gastric phenotype is correlated with the loss of key gastric genes. We investigated species from all the main gnathostome lineages and show the specific contribution of gene loss to the widespread distribution of the agastric condition. We establish that the stomach loss correlates with the persistent and complete absence of the gastric function gene kit--H(+)/K(+)-ATPase (Atp4A and Atp4B) and pepsinogens (Pga, Pgc, Cym)--in the analysed species. We also find that in gastric species the pepsinogen gene complement varies significantly (e.g. two to four in teleosts and tens in some mammals) with multiple events of pseudogenization identified in various lineages. We propose that relaxation of purifying selection in pepsinogen genes and possibly proton pump genes in response to dietary changes led to the numerous independent events of stomach loss in gnathostome history. Significantly, the absence of the gastric genes predicts that reinvention of the stomach in agastric lineages would be highly improbable, in line with Dollo's principle.
authors.affiliation: CIMAR Associate Laboratory, Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, , Porto, Portugal, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, , Porto, Portugal, Development and Evolution of Vertebrates, CNRS-UPMC-UMR 7150, , Station Biologique, Roscoff, France, Comparative Genomics Laboratory, Institute of Molecular and Cell Biology, , A*STAR (Agency for Science, Technology and Research), Biopolis, Singapore.
authors.forename: L Filipe C
authors.initials: LF
authors.lastname: Castro
authors.forename: Odete
authors.initials: O
authors.lastname: Gonçalves
authors.forename: Sylvie
authors.initials: S
authors.lastname: Mazan
authors.forename: Boon-Hui
authors.initials: BH
authors.lastname: Tay
authors.forename: Byrappa
authors.initials: B
authors.lastname: Venkatesh
authors.forename: Jonathan M
authors.initials: JM
authors.lastname: Wilson
mesh_terms: D000818:Animals; D030161:Avian Proteins / Q000737:chemistry / Q000235:genetics; D005075:Biological Evolution; D002645:Chickens / Q000033:anatomy & histology / Q000235:genetics; D029941:Fish Proteins / Q000737:chemistry / Q000235:genetics; D017353:Gene Deletion; D020440:Gene Duplication; D016678:Genome; D017506:H(+)-K(+)-Exchanging ATPase / Q000737:chemistry / Q000235:genetics*; D010802:Phylogeny; D012754:Sharks / Q000033:anatomy & histology / Q000235:genetics; D013270:Stomach / Q000033:anatomy & histology / Q000502:physiology*
chemical_list: D030161:Avian Proteins; D029941:Fish Proteins; D017506:H(+)-K(+)-Exchanging ATPase
keywords: gene duplication; gene loss; gnathostomes; pepsinogen; proton pump; stomach