Adaptive phylogeography: functional divergence between haemoglobins derived from different glacial refugia in the bank vole
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1 Electronic supplementary material for: Adaptive phylogeography: functional divergence between haemoglobins derived from different glacial refugia in the bank vole Petr Kotlík, Silvia Marková, Libor Vojtek, Antonín Stratil, Vlastimil Šlechta, Pavel Hyršl and Jeremy B. Searle Supplementary figures Rodent phylogeny Rattus Mus Peromyscus Clethrionomys Coding sequence Rattus HBB-T3 87 Rattus HBB-T4 99 Rattus HBB-T2 85 Rattus HBB-T1 Mus HBB-T1 95 Mus HBB-T2 100 Peromyscus HBB-T Peromyscus HBB-T2 Clethrionomys HBB-T1 Clethrionomys HBB-T ' Untranslated region Rattus HBB-T1 99 Rattus HBB-T3 100 Rattus HBB-T2 97 Mus HBB-T1 Peromyscus HBB-T1 82 Clethrionomys HBB-T1 87 Rattus HBB-T4 97 Mus HBB-T2 82 Peromyscus HBB-T2 Clethrionomys HBB-T Figure S1. Orthologous relationships of the two bank vole (Clethrionomys) β-globin genes with those of house mouse (Mus), rat (Rattus) and deer mouse (Peromyscus). Separate maximum likelihood trees were constructed for the coding region sequences and for the sequences of the 3 untranslated region. While the phylogeny of the 3 untranslated region of each gene reflects the relationships between the species, the coding region sequences group together the paralogous genes from each species to the exclusion of the orthologous genes from the other species, likely due to a history of interparalog gene conversion. The HBB-T4 gene of rat is orthologous to HBB-T2 genes of house mouse, deer mouse and bank vole, while the HBB-T2 and HBB-T3 genes of rat are duplicates specific to this species [1]. Numbers along branches indicate the percent bootstrap frequencies. 1
2 Figure S2. Protein analysis of bank vole haemoglobin. (a) Precipitated globin polypeptides separated by urea-cellulose acetate electrophoresis demonstrating the β-globin polymorphism underlying Hb S and Hb F. Polypeptides encoded by HBA-T3 are not visible on this gel due to the low expression level. (b) Disulphide-mediated polymerization of Hb F, but not of Hb S, following thiol oxidation by diamide. The formation of the high-molecular-weight smear during starch-gel electrophoresis of the Hb F haemolysate, accompanied by a loss of the major band corresponding to tertrameric Hb, is reversed by 2-mercaptoethanol (2-ME), a disulphide-reducing agent. 2
3 Northern Cline Southern Devon Haplotype with conversion tract Ser52Cys Ser52Cys HBB-T1 HBB-T2 HBA-T1 HBA-T2 HBA-T3 Figure S3. Haplotype relationships for each bank vole α- and β-globin gene. Circle area is proportional to haplotype frequency, and circles are coded according to the presence of each haplotype at localities north of, south of, and within the haemoglobin frequency cline (figures 1 and S4), with Devon coded separately from other southern localities. Loops in the networks represent homoplasies, including possible recombination events. The Ser52Cys change is shown as black boxes and all other amino acid replacements as open boxes across branches. The Ser52Cys mutation is homoplasious in the HBB-T1 network and the dotted line connects its alternative occurrences. 3
4 1 0.8 Hb S frequency NYK YOR DNC Latitude ( N) Figure S4. Geographic cline of haemoglobin frequency plotted along latitude. The cline shape was estimated by fitting an asymmetric stepped model in ClineFit (for details see main text). The three localities in the cline are labelled according to table 1 and figure 1. 4
5 Supplementary tables Table S1. The origin of the samples and the frequency of the haemoglobin Hb F at each locality. code county/city country latitude longitude n Hb F frequency ABD Aberdeenshire Scotland HLD Highland Scotland AGB Argyll and Bute Scotland MLN Midlothian Scotland NYK North Yorkshire England YOR York England DNC Doncaster England CAM Cambridgeshire England GLS Gloucestershire England CON1 Cornwall England DEV Devon England CON2 Cornwall England
6 Table S2. Conserved mammalian primers used for PCR amplification from cdna. genes primer sequence reference α-globin PIKAHbA-F CTTCCCCACCACCAAGACCTAC [2] PIKAHbA-R TTAACGGTRTTTGGAGGTCAGC [2] β-globin PIKAHbB-F GAGGCCCTGGGCAGGCTGCTGG [2] PIKAHbB-R CCAGGAGCCTGAAGTTCTCAGG [2] Table S3. Bank vole primers used for RACE PCR. genes end primer sequence reference α-globin 5 RACE GSP4HBA AACGGTACTTGGAGGTCAGCACGGT this study 3 RACE GSP6HBA TGCGTGTGGACCCTGTSAACTTCAAGCTC this study β-globin 5 RACE GSP1_1HBB TGTCCAGGTGTTTCAGGCCGTCACCAAAGG this study 3 RACE GSP2_1HBB AGGTTCTTTGAACACTTTGGGGACCTG this study 6
7 Table S4. Paralogous gene-specific primer pairs used for PCR amplification and sequencing of bank vole globin genes from genomic DNA. genes paralog primer sequence reference α-globin HBA_T1 HBA1F20mis ACACACTTCTGATTCTGAGA this study D-2387R CAAAGACCAAGAGGTACAG [3] HBA_T2 D-1518 CTTGCTCTGCAGCGCACC [3] D-2387R CAAAGACCAAGAGGTACAG [3] HBA_T3 HBA17F21 CGGACTCAGGAAGGAATTCAT this study D-2387R CAAAGACCAAGAGGTACAG [3] β-globin HBB_T1 BT1F1 ACAYTTGCTTCTGACATAGT this study BT1R593 TGAAAGTAAATGCCTTTTATTAGT this study HBB_T2 MUS_BG_3'_F2 CTAGATGCCCAAAGGTCTTC [4] MUS_BG_3'_R2 GCCTGTGCCATAGCCACC [4] HBB10U19 ATGCACACCCTGGAATTGG this study HBB1266L21 GTGCATAAACACGAGCAAGAA this study 7
8 Table S5. Composite genotype frequencies for β-globin variants segregating at the HBB-T1 and HBB-T2 genes. HBB-T1 (site 52-site 58) HBB-T2 (site 52) ABD HLD AGB MLN NYK YOR DNC CAM GLS CON1 DEV CON2 Total Ser-Ala/Ser-Ala Ser/Ser Ser-Ala/Ser/Val Ser/Ser 1 1 Ser-Ala/Cys-Ala Ser/Ser Ser-Ala/Cys-Ala Ser/Cys 1 1 Ser-Ala/Cys-Val Ser/Ser 1 1 Ser-Val/Cys-Ala Ser/Ser Cys-Ala/Cys-Ala Ser/Ser Cys-Ala/Cys-Ala Ser/Cys Cys-Ala/Cys-Ala Cys/Cys Cys-Ala/Cys-Val Ser/Ser Cys-Ala/Cys-Val Ser/Cys Cys-Ala/Cys-Val Ser/Cys 1 1 Cys-Val/Cys-Val Ser/Ser
9 Table S6. RNA-seq expression levels of the two β-globin genes for three bank voles possessing different haemoglobin variants. haemoglobin variant HBB-T1 RPKM a HBB-T2 RPKM fold difference Z-test statistics p-value Hb S 1,528,574 80, <0.001 Hb F 1,558,147 51, <0.001 b Hb F/Hb S min 1,543,012 66, <0.001 a reads per kilobase per million mapped reads b individual with HBB-T2 encoding a minor β-chain isoform structurally identical to Hb S References 1. Hoffmann FG, Opazo JC, Storz JF New genes originated via multiple recombinational pathways in the β-globin gene family of rodents. Mol Biol. Evol. 25, Yingzhong Y YC, Guoen J, Zhenzhong B, Lan M, Haixia Y, Rili G Molecular cloning and characterization of hemoglobin alpha and beta chains from plateau pika (Ochotona curzoniae) living at high altitude. J. Biochem. Mol. Biol. 40, Storz JF, Sabatino SJ, Hoffmann FG, Gering EJ, Moriyama H, Ferrand N, Monteiro B, Nachman MW The molecular basis of high-altitude adaptation in deer mice. PLOS Genet. 3, Storz JF, Baze M, Waite JL, Hoffmann FG, Opazo JC, Hayes JP Complex signatures of selection and gene conversion in the duplicated globin genes of house mice. Genetics 177,
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