Abstract

The family of secretory calcium-binding phosphoproteins (SCPPs) have been considered vital to skeletal tissue mineralization. However, most previous SCPP studies focused on phylogenetically distant animals but not on those closely related species. Here we provide novel insights into the coevolution of SCPP genes and fish scales in 10 species from Otophysi. According to their scale phenotypes, these fishes can be divided into three groups, i.e., scaled, sparsely scaled, and scaleless. We identified homologous SCPP genes in the genomes of these species and revealed an absence of some SCPP members in some genomes, suggesting an uneven evolutionary history of SCPP genes in fishes. In addition, most of these SCPP genes, with the exception of SPP1, individually form one or two gene cluster(s) on each corresponding genome. Furthermore, we constructed phylogenetic trees using maximum likelihood method to estimate their evolution. The phylogenetic topology mostly supports two subclasses in some species, such as Cyprinus carpio, Sinocyclocheilus anshuiensis, S. grahamin, and S. rhinocerous, but not in the other examined fishes. By comparing the gene structures of recently reported candidate genes, SCPP1 and SCPP5, for determining scale phenotypes, we found that the hypothesis is suitable for Astyanax mexicanus, but denied by S. anshuiensis, even though they are both sparsely scaled for cave adaptation. Thus, we conclude that, although different fish species display similar scale phenotypes, the underlying genetic changes however might be diverse. In summary, this paper accelerates the recognition of the SCPP family in teleosts for potential scale evolution.

Highlights

  • Phenotypic variations underlying the genetic differences between species are cryptic and attractive for biologists

  • The functions of secretory calcium-binding phosphoprotein (SCPP) genes in determining scale phenotypes need to be further verified in sparsely scaled fishes. No such studies are available currently. This present study focuses on the SCPP repertoire in 10 fishes, including A. mexicanus, Ctenopharyngodon idellus (CI; grass carp), Cyprinus carpio (CC; common carp), Ictalurus punctatus (IP; Channel catfish), Leuciscus waleckii (LW; Amur ide), Pimephales promelas (PP; fathead minnow), Pygocentrus nattereri (PN; red-bellied piranha), Sinocyclocheilus anshuiensis (SA), Sinocyclocheilus grahamin (SG), and Sinocyclocheilus rhinocerous (SR)

  • After comparing the SCPP gene copies, we estimated that the fourth whole-genome duplication (WGD) in Cyprininae with a high possibility caused the duplication of SPARCL1 and SCPP genes

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Summary

Introduction

Phenotypic variations underlying the genetic differences between species are cryptic and attractive for biologists. The secretory calcium-binding phosphoprotein (SCPP) family have attracted special attention, mainly due to their crucial functions in the mineralization of bone, dentin, enamel, and enameloid, which are beneficial to vertebrates’ protection, predation, and locomotion [2,3,4]. These genes arose from gene duplication and originated from a common ancestor, SPARCL1 (the secreted protein, acidic, cysteine-rich like 1).

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