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Gen Comp Endocrinol. 2019 Aug 1;279:139-147. doi: 10.1016/j.ygcen.2019.02.022. Epub 2019 Mar 2.

Revisiting the evolution of the somatostatin family: Already five genes in the gnathostome ancestor.

Author information

1
Physiologie moléculaire et adaptation UMR 7221 CNRS and Muséum National d'Histoire Naturelle, Paris, France. Electronic address: htostivi@mnhn.fr.
2
Physiologie moléculaire et adaptation UMR 7221 CNRS and Muséum National d'Histoire Naturelle, Paris, France.
3
Biologie intégrative des organismes marins, UMR 7232 CNRS, Observatoire Océanologique, Sorbonne Université, Banyuls-sur-Mer, France.

Abstract

The somatostatin (SST) family members are a group of neuropeptides that are best known for their role in the regulation of growth, development and metabolism. The occurrence of six paralogous SST genes named SST1, SST2, SST3, SST4, SST5 and SST6 has been reported in vertebrates. It has been proposed that SST1, SST2 and SST5 arose in 2R from a common ancestral gene. SST3 and SST6 would have been subsequently generated by tandem duplications of the SST1 and SST2 genes respectively, at the base of the actinopterygian lineage. SST4 is thought to have appeared more recently from SST1, in teleost-specific 3R. In order to gain more insights into the SST gene family in vertebrates, we sought to identify which paralogs of this family are present in cartilaginous fish. For this purpose, we first searched the recently available genome and transcriptome databases from the catshark Scyliorhinus canicula. In a previous study, three S. canicula SST genes, called at that time SSTa, SSTb and SSTc, were identified and proposed to correspond to SST1, SST5 and SST2 respectively. In the present work, two additional SST genes, called SSTd and SSTe, were found in S. canicula plus two other chondrichtyan species, elephant shark (Callorhinchus milii) and whale shark (Rhincodon typus). Phylogeny and synteny analyses were then carried out in order to reveal the evolutionary relationships of SSTd and SSTe with other vertbrates SSTs. We showed that SSTd and SSTe correspond to SST2 and SST3 respectively, while SSTc corresponds to SST6 and not to SST2 as initially proposed. Our investigations in other vertebrate species also led us to find that the so-called SST2 gene in chicken, lungfish, sturgeons and teleosts actually corresponds to SST6. Conversely, the so-called SST6 gene in actinopterygians corresponds to SST2. Taken together, our results suggest that: i) SST3 and SST6 were already present in the gnathostome ancestor, much earlier than previously thought; ii) SST6 was also present in the tetrapod ancestor and still occurs in living birds; with this respect, it is likely that SST6 was independently lost several times during evolution: in amphibians, squamates and mammals; iii) SST2, SST3 and SST5 were probably lost in euteleosts, sarcopterygians and tetrapods, respectively.

KEYWORDS:

Cartilaginous fish; Chondrichthyes; Elasmobranchii; Evolution; Holocephali; Multigenic family; Neuropeptides; Somatostatin; Vertebrates

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