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.
Proc Biol Sci. 2013 Dec 4;281(1775):20132669. doi: 10.1098/rspb.2013.2669. Print 2014 Jan 22.
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.
胃是有颌类进化的标志，代表了一种独特的解剖学创新，其特征是存在分泌酸和胃蛋白酶的腺体。然而，这些腺体在有颌类物种中的出现并非普遍存在；19 世纪，法国动物学家居维叶首次指出，一些硬骨鱼没有胃。引人注目的是，海龙目（鲨鱼和鳐鱼）、肺鱼（肺鱼）和单孔目动物（产卵哺乳动物）也缺乏胃酸分泌和胃细胞表型。在这里，我们检验了胃表型缺失与关键胃基因缺失相关的假设。我们研究了来自所有主要有颌类谱系的物种，并展示了基因缺失对广泛分布的无胃状态的特定贡献。我们确定胃的缺失与胃功能基因试剂盒的持续和完全缺失相关，该试剂盒包括 H(+)/K(+)-ATPase（Atp4A 和 Atp4B）和胃蛋白酶原（Pga、Pgc、Cym），在分析的物种中。我们还发现，在有胃的物种中，胃蛋白酶原基因的组成变化很大（例如，硬骨鱼中有两个到四个，而一些哺乳动物中有几十个），并且在不同的谱系中鉴定出了多个假基因化事件。我们提出，胃蛋白酶原基因和可能的质子泵基因在对饮食变化的适应过程中，选择压力的放松导致了有颌类历史上胃的多次独立缺失事件。重要的是，胃基因的缺失表明，在无胃的谱系中重新发明胃的可能性非常小，这符合多洛定律。
