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You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. A Publisher Correction to this article was published on 09 December 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 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.Do THIS to be DOMINANT in BED (BDSM Story Time)
Our 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.
Differential selection on male and female individuals in sexual antagonism, with profound implications for genome evolution, adaptation and the maintenance of fitness variation 1234. While this model explains sexual conflict resolution in some species, many taxa lack morphologically differentiated sex chromosomes 5 ; how sexually antagonistic variation is maintained in these species is largely unknown 47.
Additionally, recent theoretical work has predicted that sexual conflict may be better resolved by autosomal variation 8a prediction supported by genome-wide mapping of sexually antagonistic polymorphisms 3. Thus, mechanisms that maintain sexual conflict polymorphisms on the autosomes must be common, yet the only known such mechanism—sex-dependent dominance reversal 79where the favourable allele in each sex is dominant in that sex—has been observed only for a single maturity gene in Atlantic salmon 4 and for genome-wide variation for fitness in seed beetles As a result, the mechanisms maintaining sexually antagonistic variation in the absence of differentiated sex chromosomes and their consequence for adaptive and genome evolution are unresolved.
Autosomal inversion supergenes controlling alternative reproductive tactics and resembling sex chromosomes have been identified in some taxa, but typically suffer from homozygous lethality 1112 and concomitant chromosomal degradation 13 Balancing selection can facilitate the evolution of new dominance patterns and these, along with epistasis, are important features of inversion polymorphisms 15 Typical of taxa with homomorphic sex chromosomes 5817salmonids have undergone frequent sex chromosome turnover 18and sex-reversed males XY females have been suggested to occur 1920both of which are predicted to limit divergence of the sex chromosomes 521 and their ability to accumulate and protect sexual conflict polymorphisms 8 Oncorhynchus mykiss rainbow trout is a salmonid fish species that expresses two contrasting life-history strategies: resident rainbow trout live entirely in freshwater, while anadromous steelhead trout migrate to the ocean to mature, returning to freshwater to reproduce.
Survival of migratory juveniles to adulthood is very low, but fecundity of anadromous females can exceed that of resident females by an order of magnitude In contrast, males can mature early as freshwater residents, avoiding the high mortality associated with marine migration and employing a sneaker mating strategy to access paternity This sex-specific trade-off between reproduction and survival in a greater frequency of anadromy in females 23 and may drive sexual conflict over alternative migratory tactics with a shared genetic basis.
work has identified a major effect locus on chromosome Omy05 that associates with migratory phenotypes 2425but the structure and composition of this region as well as its ability to resolve sexual conflict are unknown. Here we generate a chromosome-level genome assembly for rainbow trout and use it to characterize a large autosomal inversion supergene on Omy05, and show that it mediates sexual conflict over migratory tendency via sex-dependent dominance reversal. Lacking homozygote lethality, this inversion complex provides a mechanism for maintaining polygenic sexually antagonistic variation while avoiding the deleterious mutation load accumulated by differentiated sex chromosomes.
High-density linkage analysis, based on the mapping of 46, single-nucleotide polymorphisms SNPs in a pedigree of full-sib families with 5, individuals, together with long-range data from the Dovetail Genomics Chicago library sequencing 30was used to order and orient 7, scaffolds within linkage groups, producing 29 chromosome-length sequences containing 1.
Overall, repetitive sequences for Analysis of homeologous regions resulting from the salmon-specific duplication revealed 88 collinear blocks along 29 chromosomes Fig. The red rectangles represent blocks of sequences without identifiable duplicated regions elsewhere in the genome. Linkage mapping detailed striking recombination differences between the sexes across the genome Fig. Haplotypes tagging these rearrangements were identified and used to classify the parents of the mapping families. Subsequent linkage mapping in homozygous parent families disclosed the structure of the inversions, while linkage mapping in families from heterozygous parents documented almost complete repression of recombination across the rearrangements Extended Data Fig.
The Omy05 rearrangement is characterized by two adjacent inversions of The alternative karyotypes in the Omy05 double inversion were categorized as ancestral A or rearranged R based on their sequence and structural synteny relative to the Atlantic salmon, coho salmon and Arctic char genomes, and linkage maps for Chinook, chum and sockeye salmon Extended Data Fig. Because the draft genome assembly was made from a homozygous RR individual, we generated a second genome assembly for a male homozygous for the ancestral karyotype using long-read nanopore sequencing to determine more exact breakpoints for the Omy05 rearrangements Extended Data Fig.
The Omy20 inversion region is smaller, approximately These indicate two large inversions, the first of which is pericentromeric, meaning it moves the centromere the black circle at base of the plot. Key candidate genes with related functions are spread across the two inversions; the colours depict trait-relevant functions. The purple s indicate locations where whole-genome resequenced individuals were selected. A sharp rise in divergence occurred at the inversion boundaries coincident with the breakpoints in the linkage map, with maximal divergence in the pericentromeric region peaking in a 2.
This pericentromeric region also displays a pronounced decrease in sequence diversity Fig. Dating of coding sequence CDS divergence across the inversions suggested that they have been maintained for approximately 1. There was no evidence for different ages of the two inversions, leaving the order of occurrence unresolved. Furthermore, no evidence of differences in the dating estimates was found between the centre and inversion breakpoints either from the dating of coding regions or F STconsistent with the double inversion forming a very strong barrier to recombination. Sex-specific migratory optima are expected to result in intra-locus sexual conflict in rainbow trout where there is a shared genetic basis to migratory tendency.
studies have associated genetic markers on Omy05 with migratory traits in rainbow trout 2425 ; thus, the double inversion could potentially have sex-specific effects on life history. Therefore, we tested the role inversion karyotype plays in mediating sexual conflict and whether sex-dependent dominance contributes to its resolution. Such asymmetric sex-dependent dominance reversal is predicted when the strength of antagonistic selection differs between the sexes 9and has also been observed in age at maturity in Atlantic salmon 4.
The observed sex-dependent dominance reversal of the Omy05 double inversion and its role in resolving sexual conflict over migratory tendency could reflect the homeology between the centromeric half of the sex chromosome Omy 0— However, it is unknown what role, if any, the sex chromosomes of rainbow trout play in sexual conflict resolution. The sex-determining locus, sdY 32of salmonids including rainbow trout, is located within a transposon cassette, leading to frequent chromosome turnover and a lack of homology among sex chromosomes throughout the family and within Atlantic salmon 20 Theory predicts sex chromosome translocations to be driven by the need to resolve sexual conflict or avoid mutation load accumulation 3435but the frequent turnover of salmonid sex chromosomes may limit their capacity to protect sexual conflict polymorphisms relative to typical heteromorphic sex chromosomes 5.
Because even homomorphic sex chromosomes may be differentiated at the molecular level 36we next tested for atures of divergence and the accumulation of sexually antagonistic variation in the rainbow trout sex chromosome, Omy29, to determine if homeology with the sex chromosome could explain the apparent role played by the Omy05 supergene in sexual conflict resolution. Elevated genetic differentiation F ST between the sexes is predicted around sexually antagonistic loci in linkage disequilibrium with the sex determiner It is noteworthy that this region is highly rearranged, creating a barrier to homeologue recombination with Omy29 Extended Data Figs.
Linkage analysis confirmed that male recombination is strongly localized towards the telomere on Omy29 Fig. Thus, if XY divergence is limited only by recombination in males, divergence should be seen across most of the Y chromosome. In contrast, divergence was largely restricted to the region between sdY and the centromere, where recombination is also low in females Fig. Red lines denote the 0. To test for enrichment of genes on Omy29 with sex-specific effects, we defined male and female benefit genes as those with maximum expression in testis and oocyte, respectively, compared to a panel of 13 somatic tissues.
Conversely, low recombination between X and Y with weak sexual antagonism can lead to feminization of the Y chromosome 8. These were further supported by the similar distributions of sequence coverage between males and females, consistent with the Y chromosome not having gained or retained genes not present on the X chromosome Fig. The symmetrical levels of gene loss between the Y chromosome and its autosomal orthologue in coho salmon, Oki29 ref.
Finally, we found little evidence of structural rearrangements on Omy29 that are predicted to accompany Y chromosome recombination shutdown Together, the absence of XY differentiation, sex-biased gene enrichment, rearrangements or other als predicted by the classical model of sex chromosome evolution 56 suggest that selection against deleterious mutation load, rather than the resolution of sexual conflict 1721has driven Y chromosome evolution in rainbow trout.
In contrast, the absence of homozygote lethality of either karyotype of the Omy05 inversion allows within-karyotype recombination to purge deleterious mutations, thus avoiding degradation. Thus, sex-dependent dominance reversal of the Omy05 rearrangement provides an alternative autosomal mechanism to resolve sexual conflict while avoiding the mutation load associated with the canonical heteromorphic sex chromosome system. Inversion supergenes allow coadapted variants to avoid being broken up by recombination The Mb double inversion on Omy05 contains 1, protein-coding genes; a single causative gene or mutation is probably not responsible for the observed phenotypic association.
Visual-related pathways are known to be overrepresented among genes differentially expressed between resident and anadromous rainbow trout 45reflecting the importance of light in the timing of smoltification and maturation. The inversion includes the master regulator of circadian rhythm, CLOCKand the visual pigment, OPN4, which is expressed in the saccus vasculosus, the organ that controls photoperiodism and so reproductive timing in fish The homeologous regions of CLOCK and MAPK10 on Omy01 and Omy12, respectively, have ly been implicated in migratory phenotypes in northern populations 5253supporting a role for these genes in trait divergence and suggesting that selection on gene duplicates may contribute to a more diffuse architecture in the north, independent of the Omy05 inversion.
Notably, DMRTA2 is a duplicate of the sexual dimorphism gene Doublesex 54which is expressed in the developing gon and pituitary 5556 with greater adult expression in the testes than ovaries of teleost fish 57 In zebrafish, DMRTA2 regulates terminal differentiation of corticotropes and gonadotropes, through which it may accelerate gonadal development and so influence maturation timing DMRTA2 regulates cells expressing pro-opiomelanocortin pomc 55which is differentially expressed between migratory forms of rainbow trout 45 and Atlantic salmon DMRTA2 and pomc are also differentially expressed in rx3 mutant zebrafish 60resulting in disrupted circadian rhythm Two other genes known to have strong sex-specific effects and to affect maturation are found in the inversion AMHa gene involved in the differentiation of rainbow trout gon 6162and NR5A2which is involved in oestrogen biosynthesis and inhibition of adipogenesis through its regulation of CYP19a1 refs.
This is important because adiposity is a key determiner of migratory behaviour that is strongly and consistently associated with divergent migratory and maturation phenotypes in salmonid fish 42265 Finally, neighbouring CLOCK is KITwhich regulates melanocytes 73potentially contributing to the transition from melanic riverine to silvery migratory colouration during smoltification Fig. The presence of this assemblage of interrelated genes supports the Omy05 inversion as a supergene with sex-dependent effects on migratory tendency in rainbow trout.
The frequency of the rearranged karyotype varied with migratory access in 91 geographically distributed population samples mean R frequency above versus below barriers, 0. These patterns are probably driven by temperature-dependent developmental rates 2274major quantitative trait loci which overlap the Omy05 rearrangement 245374strongly predict reproductive timing and early male sexual maturation In these colder, high-latitude populations, the faster intrinsic developmental rate required to compensate for the effects of decreased temperature may result in positive selection for the rearranged karyotype irrespective of migratory phenotype Fig.
However, anadromy is also rarer at high latitudes, reflecting both the increased food availability in rivers with large salmon runs and increased accumulation of adipose tissue with lower metabolic rates in cooler rivers 22 These trends reduce the cost of residency for females, suggesting a concomitant decrease in sexual antagonism and that sexual conflict resolution by sex-dependent dominance is dependent on geographical variation in the strength of sex-specific selection 14 Fish silhouettes provided by J.
Moore, used with permission. Differences in development, fecundity and relative expression of alternative life-history patterns are influenced by environment temperature, developmental rate, selection by migration barrierssex, and Omy05 karyotype, leading to the alternative individual migratory life histories known as rainbow trout and steelhead. Inversion supergenes maintained by balancing selection have been associated with the evolution of new dominance patterns, and unlinked modifiers are thought to act epistatically on inversion effects 1544 Our demonstrate sex-dependent dominance reversal of an autosomal inversion contributing to the resolution of sexual conflict over a complex life history trade-off.
Sex-dependent dominance of the higher fitness karyotype within each sex provides the conditions for net heterozygote superiority 7allowing independent optimization of the migratory phenotype in both males and females and the maintenance of sexual conflict polymorphisms over a large chromosomal segment. In stark contrast, the Y chromosome lacks atures typical of sex chromosome evolution, with no evidence for enrichment of male benefit genes, isolating structural rearrangements or an excess of gene loss indicative of degeneracy.
These patterns strongly suggest that Y chromosome evolution in rainbow trout is driven primarily by the avoidance of mutation load, with limited capacity to maintain sexual conflict polymorphisms and that the Omy05 rearrangement represents an autosomal alternative to the canonical model of sexual conflict resolution by sex chromosomes.
Linkage is expected to both develop in sexually antagonistic loci and to relax the conditions for maintenance of sexually antagonistic variation because of increased fitness effects Such processes can lead to the accumulation of loci with large fitness effects predicted under sexual antagonism 79 ; thus, the sex-dependent dominance reversal of an autosomal supergene we observe in rainbow trout may represent a common mechanism for the maintenance of polygenic sexually antagonistic variation.
In contrast to other inversions underlying alternative reproductive tactics 11121314lack of homozygous lethality enables the Omy05 rearrangement to purge deleterious mutations from both karyotypes. The inversion complex has been maintained by sexually antagonistic balancing selection for approximately 1. However, this architecture is probably geographically variable, with selection on temperature-dependent developmental rate and the strength of sexual antagonism over alternative migratory tactics changing with latitude.Local sex dominant
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Sex-dependent dominance maintains migration supergene in rainbow trout