Males and females often differ in their fitness optima for shared traits that have a shared genetic basis, leading to sexual conflict. Morphologically differentiated sex chromosomes can resolve this conflict and protect sexually antagonistic variation, but they accumulate deleterious mutations. However, how sexual conflict is resolved in species that lack differentiated sex chromosomes is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 55-Mb double-inversion supergene that mediates sex-specific migratory tendency through sex-dependent dominance reversal, an alternative mechanism for resolving sexual conflict. The double inversion contains key photosensory, circadian rhythm, adiposity and sex-related genes and displays a latitudinal frequency cline, indicating environmentally dependent selection. Our results show sex-dependent dominance reversal across a large autosomal supergene, a mechanism for sexual conflict resolution capable of protecting sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutations associated with typical heteromorphic sex chromosomes.
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The reference genome assembly: GenBank Assembly Accession GCA_002163495.1, RefSeq Assembly Accession GCF_002163495.1. Raw sequence data used for the genome assembly: NCBI SRA Accession SRP086605 (Project ID: Project PRJNA335610). Raw sequence data used for whole-genome resequencing: NCBI SRA Accession SRP107028 (Project ID: PRJNA386519). New RNA-seq data generated for the genome annotation: NCBI SRA Accession SRP102416 (Project ID: PRJNA380337). Additional sequence data used for the NCBI RefSeq annotation are listed and described at https://www.ncbi.nlm.nih.gov/genome/annotation_euk/Oncorhynchus_mykiss/100/. Raw sequence data used for generating RAD SNP markers that were used for anchoring assembly scaffolds and contigs to chromosomes: USDA: NCBI SRA Accession SRP063932 (Project ID: PRJNA295850); UC Davis: NCBI SRA Accession SRP141092 (Project ID: PRJNA450873). NMFS data and analysis can be found at https://github.com/eriqande/Pearse_etal_NEE_NMFS_Data_Analysis.
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We thank H. Fish, K. Pipal and many others for help with fieldwork; V. Apkenas, A. Carlo and E. Campbell for assistance with data collection and analysis; and M. Readdie and F. Aryas for support at the University of California Landels-Hill Big Creek Reserve. Samples and data for the geographic survey were provided by M. Ackerman, S. Lewis, S. Narum, K. Nichols, S. Northrup (Freshwater Fisheries Society of British Columbia), E. Taylor (University of British Columbia), D. Teel and K. Warheit. Compute Canada provided the computing resources used in repeat annotation and analysis. We thank R. Long and K. Shewbridge for their help in DNA sample preparation for sequencing and genotyping and in the preparation of RAD-seq libraries, and K. Martin and Troutlodge for the permission to use samples from their germplasm for genotyping. We also thank the Genomics Core at Washington State University, Spokane, the University of Idaho Genomics Core and the Vincent J. Coates Genomics Sequencing Laboratory at University of California, Berkeley for performing DNA library preparation and clonal lines’ resequencing. The genome resequencing of the Whale Rock female clonal line was conducted in collaboration with M. Garvin, Oregon State University. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer. This project was supported by funds from the USDA-ARS (in-house project nos. 1930-31000-009 and 8082-31000-012). DH clonal line resequencing was supported by an Agriculture and Food Research Initiative Competitive Grant (no. 2015-07185) from the USDA National Institute of Food and Agriculture and by an NRSP8 Aquaculture Genome funding seed grant to M.G. and G.T. The whole-genome resequencing data provided by K. Naish was obtained from a project supported by an Agriculture and Food Research Initiative Competitive Grant (no. 2012-67015-19960) from the USDA National Institute of Food and Agriculture. Funding for bioinformatics and statistical support at CIGENE (Norwegian University of Life Sciences) was provided by NFR grants (nos. 208481, 226266 and 275310). Bioinformatics analyses were performed using resources at the Orion Computing Cluster at CIGENE, with storage resources provided by the Norwegian National Infrastructure for Research Data (project no. NS9055K). We acknowledge the help of S. Karoliussen and M. Arnyasi at CIGENE for generating rainbow trout genotypes and M. Baranski for work on the genetic linkage maps. C. R. Primmer and K. Nichols provided valuable comments on the draft manuscript.
The authors declare no competing interests.
Animal use All animal handling was conducted in accordance with approved institutional guidelines.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended Data Fig. 1 Activity periods, abundance, and historical proliferation of Tc1-Mariner families in Atlantic salmon, rainbow trout, and Chinook salmon.
a. Lower sequence similarity between family members indicates a more ancient family. Activity and abundance are generally consistent among the three species until the time corresponding to ~ 93% sequence similarity, after which substantial differences in activity have occurred in concert with salmonid lineage divergence. Tc1-Mariner families displayed were identified in Atlantic salmon and rainbow trout and occupied at least 0.1% of the genome in one of the three species. b. Stacked density plot of pairwise similarity between Tc1-Mariner family members. The large initial peak with a maxima at ~86% corresponds roughly to the same time that the salmonid-specific whole-genome duplication took place. In the time corresponding to more than 93% similarity, differences in activity begin to appear between Atlantic salmon and rainbow trout in accordance with their ancestral divergence (compare to Fig. 3a in Lien et al, 2016).
Extended Data Fig. 2 High-density linkage maps describing characteristic sex-specific recombination patterns and resolving variable chromosome numbers associated with centric fusions or fissions in rainbow trout.
a. Linkage map for the metacentric rainbow trout chromosome 8 (Omy08) demonstrating male recombination strongly localized towards both telomeres and female recombination repressed at the centromere. b. Linkage map for the metacentric rainbow trout chromosome 2 (Omy02) demonstrating elevated male recombination towards the telomeric region at the q-arm but repressed recombination at the p-arm typified by showing high sequence similarity to Omy03p. c. Linkage map for the acrocentric rainbow trout chromosome 29 (Omy29) with the sex-determining gene sdY located around 5 Mb demonstrating repressed male recombination for most of the chromosome except the telomeric region. d.-f. Rainbow trout chromosomes with variable chromosome numbers associated with centric fusions or fissions. Gaps in the linkage map at the centromere of Omy04, Omy14 and Omy25 are caused by fissions splitting metacentric chromosomes into two acrocentric chromosomes in some families.
a. Ancestral (A) versus rearranged (R) chromosomal positions showing structure of inversion complexes on Omy05 and Omy20. b. Genetic linkage maps constructed for parents with alternate Omy05 and Omy20 haplotypes. Red line; female map for homozygous ancestral (AA) parents. Blue line; male map for homozygous ancestral (AA) parents. Orange line; female map for homozygous rearranged (RR) parents with marker order as in ancestral rearrangement. Green line; female map in heterozygous parents (AR).
Extended Data Fig. 4 Chromosomal rearrangements on rainbow trout chromosome 5 (Omy05) and conserved synteny with other salmonid species.
a. Ancestral (A) or rearranged (R) haplotypes on Omy05 characterized by two adjacent inversions of 22.83 and 32.94 Mb. B. Linkage map of recombination on chromosome Omy05 in males (green) and females (red). c.The alignment of Omy05 with the rest of the rainbow trout genome assembly show conserved collinear blocks of homeology with Omy12p, Omy29, Omy01p and Omy04p. d. The alignment of Omy05 with Atlantic salmon genome assembly (GCF_000233375.1) identifies highly conserved synteny with salmon chromosomes 1 and 10 (Ssa01qb and Ssa10qa). e. Alignment with the Arctic char genome (GCF_002910315.2) detects highly conserved synteny with char chromosomes 4 and 16 (Sal04 and Sal16). f. Alignment of Omy05 with coho salmon chromosome sequences (GCF_002021735.1) reveals conserved synteny with chromosomes 23 and 13 (Oki23 and Oki13). g. Comparison of Omy05 with RAD-based linkage maps for other Pacific salmon reveal a smaller fragment at centromere of Omy05 which is rearranged in coho, Chinook, chum and sockeye compared to rainbow trout, Arctic char and Atlantic salmon, and a larger rearrangement that differentiate coho and chinook from the other salmonid species.
a. Contigs of the ancestral type spanning the three inversion break points on Omy05. The contigs were generated by long-read nanopore sequencing of a fish known to be homozygous for the ancestral configuration of the double inversion. b. Structure of the two variants of the double-inversion on Omy05 categorized as ancestral or rearranged. c. Scaffolds of the rearranged type spanning the three inversion break points on Omy05. The scaffolds were generated from the Swanson doubled haploid line known to be homozygous for the rearranged type of the double-inversion. Tables in the lower part of the figure list SNPs flanking the inversion break points, with positions in ancestral contigs or rearranged scaffolds, respectively, as well as boarders for the three break points in the ancestral type of the double-inversion.
a. Age estimates from individual gene and CDS across the inversion showing lack of a strong pattern associated with inversion break points. b. Boxplot of age estimates for all CDS and genes that passed filtering, and the difference between the two estimates. Older estimates and wider confidence intervals are obtained from CDS than those based on gene sequences. c. Plot of the number of base differences between haplotypes for gene and CDS alignments and its effect on age estimation. Despite potentially having more variants because of the inclusion of introns, the gene alignments actually have fewer base differences per haplotype on average owing to the removal of poor quality intronic alignments by Gblocks. As a result, the CDS based alignments provide more informative alignments for dating the inversion complex. d. Estimate of inversion age in 10 Mb windows across the inversion complex for CDS estimates.
Full model results from antennae detection emigration model in Big Creek, showing mean (solid lines) and SD (dotted lines) of differential size-dependent migration of males and females with AR and AA, and RR Omy05 genotypes, with smoltification peaking at ~150 mm.
Extended Data Fig. 8 Linkage maps and conserved synteny with other salmonids for rainbow trout chromosome 29 (Omy29).
a. Sex-specific linkage maps for Omy29 (red dots; female, blue dots; male) show repressed recombination in males for the majority of Omy29. Genetic differentiation between males and females (Fst) is peaking at the sdY locus located at 5 Mb (yellow triangle) but is also elevated in the region between sdY and the centromere (Black Dot at 0 Mb). b. Regions of the rainbow trout genome homeologous with Omy29. Comparative genome sequence maps show highly conserved synteny with c. Atlantic salmon chromosome 11qb (ssa11qb) and d. Arctic char chromosome Sal05. e. Comparative mapping with coho salmon genome sequence reveals two larger rearrangements, one at 10 Mb and one at 30 Mb. f. Comparison of Omy29 with RAD-based linkage maps for other Pacific salmon show that the rearrangement at 10 Mb is conserved among coho, chinook, chum and sockeye and differentiated from rainbow trout and Atlantic salmon.
Principal component (PC) analysis of genetic diversity estimated from (a) whole-genome sequence data genome-wide and, (b) within the chromosome Omy5 rearrangement. For both A and B, a random subset of 40,000 SNPs were examined from homozygous AA and RR individuals of known geographic origin and plotted with the principal components containing the most variance. Homozygous AA individuals are plotted as blue circles with homozygous RR individuals represented by red triangles, with numbers indicating geographic locations corresponding to Fig. 2d and Supplementary Information Table 4. While geographic structuring is apparent in the genome-wide SNP dataset, the inversion region separates clearly between RR and AA types with PC1 (28.76% of variation), and the subsequent second PC (7.49% of variation) corresponding to diversity within AA types. Similarly, population-level Neighbor-Joining trees of AA individuals and RR individuals from SNP survey data of homozygous AA individuals (c) and homozygous RR individuals (d) from sampled populations are depicted in a population level tree generated through chord distances. Support values for nodes with > 50% bootstrap support generated from 1,000 bootstrap replicates are indicated. Population numbers correspond to Fig. 2d and Supplementary Information Table 4.
For each month of the year below barrier North American populations of rainbow trout are plotted as mean monthly temperature (x – axis) and inversion frequency (y – axis). Points are sized proportionally to sample size (N). A weighted least squares regression is depicted with the adjusted R2 value for each month of the year.
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Pearse, D.E., Barson, N.J., Nome, T. et al. Sex-dependent dominance maintains migration supergene in rainbow trout. Nat Ecol Evol 3, 1731–1742 (2019) doi:10.1038/s41559-019-1044-6