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

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.