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Dryad

The evolution of hemocyanin genes in Tectipleura - a multitude of conserved introns in highly diverse gastropods

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Feb 02, 2021 version files 500.76 KB

Abstract

Background: Hemocyanin is the oxygen transporter of most molluscs. Thus, it is an essential protein of these animals which needs to be adapted perfectly to their environments. In Tectipleura, which is a very large and diverse gastropod group with >27,000 species living in all kinds of habitats, several hemocyanin genes have already been identified. They evolved independently from each other within different lineages due to multiple gene duplications and represent potential adaptations to different environments or lifestyles. The aim of this study is to explore the evolution of these genes by analyzing their exon-intron architectures for characteristic features indicating adaptations.

Results: We reconstructed gene architectures of ten hemocyanin genes of four species of Tectipleura: (i) Aplysia californica (ii) Lymnaea stagnalis (iii) Cornu aspersum and (iv) Helix pomatia . Their hemocyanin genes comprise 53 introns each, which is conspicuously more than in known hemocyanin genes of Cephalopoda (9-11), Vetigastropoda (15) and Caenogastropoda (28-33). The gene structures of Tectipleura hemocyanins are identical in terms of number and locations of the introns with exception of only one hemocyanin of Lymnaea stagnalis that comprises one additional intron. Deeper analyses reveal that introns which vary between gene structures of different molluscan lineages most probably evolved more recently through independent intron gains.

Conclusions: The strong conservation of the large number of introns in hemocyanin genes in Tectipleura for over 200 million years suggests a selective pressure on the gene structure. While we have not found characteristic positions or sequence motifs of introns that are conserved, it may be simply the great number of introns that offers increased possibilities of gene regulation and thus may facilitate habitat shifts, adaptive radiation and speciation. This hypothesis is supported by the increased number of introns within hemocyanin genes of Pomacea canaliculata which evolved independently from those of Tectipleura. This species belongs to Caenogastropoda, the sister group of Heterobranchia (where Tectipleura belong to) which is also very diverse and comprises species living in different habitats. Thus, our study provides first evidence that a multitude of introns may contribute to adaptive gene diversity of animals.