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Recurrent Convergent Evolution at Amino Acid Residue 261 in Fish Rhodopsin

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Recurrent Convergent Evolution at Amino Acid Residue 261 in Fish Rhodopsin Recurrent convergent evolution at amino acid residue 261 in fish rhodopsin Jason Hilla, Erik D. Enbodya, Mats E. Petterssona, C. Grace Sprehna, Dorte Bekkevoldb, Arild Folkvordc,d, Linda Laikree, Gunnar Kleinauf, Patrick Scheererf, and Leif Anderssona,g,h,1 aDepartment of Medical Biochemistry and Microbiology, Uppsala University, SE-751 23 Uppsala, Sweden; bNational Institute of Aquatic Resources, Technical University of Denmark, 8600 Silkeborg, Denmark; cDepartment of Biological Sciences, University of Bergen, 5020 Bergen, Norway; dInstitute of Marine Research, 5018 Bergen, Norway; eDepartment of Zoology, Division of Population Genetics, Stockholm University, SE-106 91 Stockholm, Sweden; fGroup Protein X-ray Crystallography and Signal Transduction, Institute of Medical Physics and Biophysics, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Charitéplatz 1, D-10117 Berlin, Germany; gDepartment of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, SE-750 07 Uppsala, Sweden; and hDepartment of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX 77843 Contributed by Leif Andersson, July 26, 2019 (sent for review May 14, 2019; reviewed by Michel Georges and Philip W. Hedrick) The evolutionary process that occurs when a species colonizes a Results new environment provides an opportunity to explore the mecha- Characterization of the Selective Sweep at the Rhodopsin Locus. The nisms underlying genetic adaptation, which is essential knowledge colonization of herring into the Baltic Sea must have happened for understanding evolution and the maintenance of biodiversity. within the last 10,000 y because this area was entirely covered Atlantic herring has an estimated total breeding stock of about 12 with ice during the last glaciation. We therefore predicted that 1 trillion (10 ) and has colonized the brackish Baltic Sea within the the adaptation at this locus may be driven by derived mutations last 10,000 y. Minute genetic differentiation between Atlantic and that we do not find in herring from the Atlantic Ocean. We Baltic herring populations at selectively neutral loci combined with calculated delta allele frequencies for alleles that showed dif- this rapid adaptation to a new environment facilitated the identifi- ferentiation between Atlantic and Baltic herring and were cation of hundreds of loci underlying ecological adaptation. A major monomorphic in the Atlantic herring. This analysis supported question in the field of evolutionary biology is to what extent such EVOLUTION an adaptive process involves selection of novel mutations with the view that the peak of association coincides with the location large effects or genetic changes at many loci, each with a small of rhodopsin (Fig. 1B). The pattern of association is consistent effect on phenotype (i.e., selection on standing genetic variation). with a hard selective sweep, in which the strength of association Here we show that a missense mutation in rhodopsin (Phe261Tyr) breaks down as a function of distance from the peak. A missense is an adaptation to the red-shifted Baltic Sea light environment. mutation Phe261Tyr in rhodopsin constitutes one of the very top The transition from phenylalanine to tyrosine differs only by the single nucleotide polymorphisms (SNPs) located at the peak of presence of a hydroxyl moiety in the latter, but this results in an association (Fig. 1B), and a second missense mutation Ile213Thr up to 10-nm red-shifted light absorbance of the receptor. Re- shows a modest delta allele frequency of about 0.3; no other markably, an examination of the rhodopsin sequences from missense mutation was found in the Atlantic or Baltic herring. 2,056 species of fish revealed that the same missense mutation has occurred independently and been selected for during at least 20 Significance transitions between light environments across all fish. Our results provide a spectacular example of convergent evolution and how Fish occupy a wide range of light environments that vary a single amino acid change can have a major effect on depending on the wavelengths absorbed by the local envi- ecological adaptation. ronment, including brackish and freshwater environments in which dissolved organic matter produces a red-shifted visual adaptation | selective sweep | convergent evolution | natural selection environment compared with marine waters. Atlantic herring colonized the brackish Baltic Sea after its formation approxi- he Atlantic herring is 1 of several marine fish species that mately 10,000 y ago, which required adaptation to a red- Thave successfully colonized the entire Baltic Sea, which shifted light environment. We show that visual adaptation to happened during the last 10,000 y and thus required rapid ad- the new light environment was achieved through a recent and aptation to the dramatic decrease in salinity from 35‰ in the rapid selective sweep on a mutation in the rhodopsin gene. Atlantic Ocean to as low as 2‰ in the inner Baltic Sea. Pre- Furthermore, this exact same amino acid change has occurred viously, whole-genome sequencing revealed hundreds of loci at least 20 separate times in fish species transitioning from showing highly significant differentiation between populations of marine to brackish or freshwater environments. This is a re- Atlantic herring (Clupea harengus harengus) and Baltic herring markable example of convergent evolution. (Clupea harengus membras) (1) (Fig. 1A and Dataset S1). We − noted that 1 of the most significant associations (P < 1 × 10 100) Author contributions: L.A. designed research; J.H., E.D.E., M.E.P., C.G.S., G.K., and P.S. performed research; D.B., A.F., and L.L. contributed new reagents/analytic tools, samples, overlaps perfectly with the rhodopsin (RHO) gene (Fig. 1A), and data; J.H., E.D.E., M.E.P., G.K., P.S., and L.A. analyzed data; and J.H., E.D.E., and L.A. encoding a light-sensitive G protein-coupled receptor, which is wrote the paper with contributions from the other authors. expressed in the rod cells of the vertebrate retina and is essential Reviewers: M.G., University of Liege; and P.W.H., Arizona State University. for vision in dim light. Compared with marine water, brackish The authors declare no conflict of interest. water contains higher concentrations of dissolved organic matter This open access article is distributed under Creative Commons Attribution-NonCommercial- that scatters short-wavelength visible light and results in a visual NoDerivatives License 4.0 (CC BY-NC-ND). environment that differs from marine water, which transmits Data deposition: The sequence reported in this paper has been deposited in the European blue light more than other wavelengths. Inspired by previous Nucleotide Archive (ENA) database (accession no. ENA PRJEB32358). literature on genetic adaptation in the rhodopsin gene in other 1To whom correspondence may be addressed. Email: [email protected]. species to variation in visual environments (2–5), we explored the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. possibility that rhodopsin is the causative gene for the strong 1073/pnas.1908332116/-/DCSupplemental. selection signal on herring chromosome 4. Published online August 26, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1908332116 PNAS | September 10, 2019 | vol. 116 | no. 37 | 18473–18478 Downloaded by guest on September 24, 2021 A D Season 36 Autumn Atlantic populations Spring/ Rhodopsin Summer 150 F261Y F 65° 10 Y 100 1 log p-value 2 27 χ 50 32 24 0 1 29 0 ° 34 Absorbance (412nm) 0 10 20 30 60 38 B 5 9 1.00 4 6 26 3 35 25 22 28 33 0.75 30 37 F261Y 17 0.50 55° 31 I213T 19 2 0.25 18 21 20 Baltic allele frequency 23 Δ 0.00 10 11 12 13 14 10° 20° 30° Chromosome 4 (Mb) C 30 Salinity (PSU) 0 1 F261Y 0 I213T Fig. 1. Signal of selection and frequencies of rhodopsin alleles in Atlantic and Baltic herring. (A) Genome-wide scan of allele frequency differences in the contrast between Atlantic and Baltic herring populations revealed a highly significant signal on chromosome 4. The genome-wide plot at the top of the panel highlights the signal containing rhodopsin; the remainder of the panel shows the signal in the context of chromosome 4. (B) Delta allele frequency of SNPs that are fixed in Atlantic populations and polymorphic in Baltic populations, and therefore novel to the Baltic populations. The location of rhodopsin is highlighted with a red line in both A and B.(C) The correlation between salinity (Upper), as a proxy for visual environment, and allele frequencies of Tyr261 and Thr213 (Lower), is shown for each population numbered on the x axis. (D) Location of herring populations in the East Atlantic and Baltic Sea used in this study (Dataset S1). Pie charts are the frequency of the Phe261Tyr mutation in each population, and label colors denote autumn- or spring-spawning pop- ulations. Absorbance values at 412 nm are derived from MODIS-Aqua satellite data (30); higher values correspond to more absorbance at 412 nm and, as a consequence, a red-shifted visual environment. Ile213Thr occurs in the same exon as Phe261Tyr, only 144 bp very high selection coefficient (s ≥ 0.2) per generation is required apart. These 2 missense mutations are absent in herring from the to generate such a rapid sweep. Similarly, we used the LD decay Atlantic Ocean, but occur in populations from the Baltic Sea, between the missense mutations and flanking markers to esti- which supports their derived status, and Phe261Tyr is fixed in mate their age, which resulted in estimates of 6,400 and 42,000 y some populations from the inner Baltic (Fig. 1 C and D). for Ile213Thr and Phe261Tyr, respectively (SI Appendix, Sup- We further explored the hard sweep associated with the rho- plementary Text: Age of the sweep and Fig.
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