PUBLICATION

Recurrent gene loss correlates with the evolution of stomach phenotypes in gnathostome history

Authors
Castro, L.F., Gonçalves, O., Mazan, S., Tay, B.H., Venkatesh, B., Wilson, J.M.
ID
ZDB-PUB-201113-1
Date
2013
Source
Proceedings. Biological sciences   281: 20132669 (Journal)
Registered Authors
Venkatesh, Byrappa
Keywords
gene duplication, gene loss, gnathostomes, pepsinogen, proton pump, stomach
MeSH Terms
  • Animals
  • Avian Proteins/chemistry
  • Avian Proteins/genetics
  • Biological Evolution*
  • Chickens/anatomy & histology
  • Chickens/genetics
  • Fish Proteins/chemistry
  • Fish Proteins/genetics
  • Gene Deletion
  • Gene Duplication
  • Genome
  • H(+)-K(+)-Exchanging ATPase/chemistry
  • H(+)-K(+)-Exchanging ATPase/genetics*
  • Phylogeny
  • Sharks/anatomy & histology
  • Sharks/genetics
  • Stomach/anatomy & histology
  • Stomach/physiology*
PubMed
24307675 Full text @ Proc. Biol. Sci.
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.
Genes / Markers
Figures
Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping