Evolution of the Jawed Vertebrate (Gnathostomata) Stomach through Gene Repertoire Loss: Findings from Agastric Species

Abstract

Independent and convergent gene loss, such as the loss of gastric enzymes (Pga, Pgc) and proton pump subunits (Atp4a, Atp4b) in monotremes and polyphyletic teleost species have been associated with the agastric phenotype - stomachs lacking gross morphology, gastric glands and acid secretion. The loss of the key gastric hormone gastrin (Gast) has been observed in monotremes, but not corroborated in agastric teleosts. Furthermore, it is unclear how this loss affects the evolution and selection of the native receptor (Cckbr), gastrin releasing peptide (Grp) and receptor (Grpr), or if there are further gene losses associated with the agastric phenotype. We investigated the evolution, selection and conservation of the gastrin physiological pathway and novel gastric genes in a broad range of gastric and agastric vertebrates. Our analyses showed no correlation between the losses of Gast and Grpr with the agastric phenotype in vertebrate lineages. We identified genes implicated in gastric mucosal maintenance and development (Gkn1, Gkn2, Tff1, Tff2, Vsig1, Anxa10) that are lost in agastric species except the echidna, which retained some of them (Gkn1, Tff2, Vsig1). Our findings demonstrate a convergent repertoire of gastric genes lost in agastric species, partial retention of gastric functionality in the echidna, and the diversified roles of gastrin pathway constituents in vertebrate lineages.