Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes
- Fabio Cortesia,b,c,1,2,
- Zuzana Musilováa,1,2,
- Sara M. Stieba,c,
- Nathan S. Hartd,e,
- Ulrike E. Siebeckf,
- Martin Malmstrømg,
- Ole K. Tørreseng,
- Sissel Jentoftg,
- Karen L. Cheneyb,
- N. Justin Marshallc,
- Karen L. Carletonh, and
- Walter Salzburgera,g
- aZoological Institute, University of Basel, Basel 4051, Switzerland; Schools of
- bBiological Sciences and
- fBiomedical Sciences and
- cQueensland Brain Institute, The University of Queensland, Brisbane 4072, Australia;
- dSchool of Animal Biology and
- eThe Oceans Institute, The University of Western Australia, Crawley 6009, Australia;
- gCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo 0316, Norway; and
- hDepartment of Biology, University of Maryland, College Park, MD 20742
-
Edited by Trudy F. C. Mackay, North Carolina State University, Raleigh, NC, and approved November 20, 2014 (received for review September 15, 2014)
Significance
Gene and whole-genome duplications are important evolutionary forces promoting organismal diversification. Teleost fishes, for example, possess many gene duplicates responsible for photoreception (opsins), which emerged through gene duplication and allow fishes to adapt to the various light conditions of the aquatic environment. Here, we reevaluate the evolutionary history of the violet-blue–sensitive opsins [short wavelength-sensitive 2 (SWS2)] in modern teleosts using next generation genome sequencing. We uncover a gene duplication event specific to the most diverse lineage of vertebrates (the percomorphs) and show that SWS2 evolution was highly dynamic and involved gene loss, pseudogenization, and gene conversion. We, thus, clarify previous discrepancies regarding opsin annotations. Our study highlights the importance of integrative approaches to help us understand how species adapt and diversify.
Abstract
Single-gene and whole-genome duplications are important evolutionary mechanisms that contribute to biological diversification by launching new genetic raw material. For example, the evolution of animal vision is tightly linked to the expansion of the opsin gene family encoding light-absorbing visual pigments. In teleost fishes, the most species-rich vertebrate group, opsins are particularly diverse and key to the successful colonization of habitats ranging from the bioluminescence-biased but basically dark deep sea to clear mountain streams. In this study, we report a previously unnoticed duplication of the violet-blue short wavelength-sensitive 2 (SWS2) opsin, which coincides with the radiation of highly diverse percomorph fishes, permitting us to reinterpret the evolution of this gene family. The inspection of close to 100 fish genomes revealed that, triggered by frequent gene conversion between duplicates, the evolutionary history of SWS2 is rather complex and difficult to predict. Coincidentally, we also report potential cases of gene resurrection in vertebrate opsins, whereby pseudogenized genes were found to convert with their functional paralogs. We then identify multiple novel amino acid substitutions that are likely to have contributed to the adaptive differentiation between SWS2 copies. Finally, using the dusky dottyback Pseudochromis fuscus, we show that the newly discovered SWS2A duplicates can contribute to visual adaptation in two ways: by gaining sensitivities to different wavelengths of light and by being differentially expressed between ontogenetic stages. Thus, our study highlights the importance of comparative approaches in gaining a comprehensive view of the dynamics underlying gene family evolution and ultimately, animal diversification.
Footnotes
-
↵1F.C. and Z.M. contributed equally to this work.
- ↵2To whom correspondence may be addressed. Email: fabio.cortesi{at}uqconnect.edu.au or zuzmus{at}gmail.com.
-
Author contributions: F.C., Z.M., K. L. Carleton, and W.S. designed research; F.C., Z.M., S.M.S., N.S.H., U.E.S., and K. L. Carleton performed research; M.M., O.K.T., and S.J. contributed new reagents/analytic tools; F.C., Z.M., S.M.S., N.S.H., U.E.S., M.M., O.K.T., S.J., K. L. Cheney, N.J.M., and K. L. Carleton analyzed data; and F.C., Z.M., and W.S. wrote the paper.
-
The authors declare no conflict of interest.
-
This article is a PNAS Direct Submission.
-
Data deposition: New SWS2 sequences, SWS2 genomic regions, and the transcriptomic raw reads of the P. fuscus reference transcriptome have been deposited in the GenBank database (accession nos. KM978043–KM978047, KP004247–KP004345, and SRX736911).
-
See Commentary on page 1252.
-
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1417803112/-/DCSupplemental.
Freely available online through the PNAS open access option.
