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Journal ArticleDOI

The Genomic Architecture and Evolutionary Fates of Supergenes.

TL;DR: In this paper, the authors synthesize recent genomic work and historical models of supergene evolution, highlighting how the genomic architecture of supergenes affects their evolutionary fate, and use forward simulations to demonstrate that differences in genomic architecture affect the degeneration of super-genes.
Abstract: Supergenes are genomic regions containing sets of tightly linked loci that control multi-trait phenotypic polymorphisms under balancing selection. Recent advances in genomics have uncovered significant variation in both the genomic architecture as well as the mode of origin of supergenes across diverse organismal systems. Although the role of genomic architecture for the origin of supergenes has been much discussed, differences in the genomic architecture also subsequently affect the evolutionary trajectory of supergenes and the rate of degeneration of supergene haplotypes. In this review, we synthesize recent genomic work and historical models of supergene evolution, highlighting how the genomic architecture of supergenes affects their evolutionary fate. We discuss how recent findings on classic supergenes involved in governing ant colony social form, mimicry in butterflies, and heterostyly in flowering plants relate to theoretical expectations. Furthermore, we use forward simulations to demonstrate that differences in genomic architecture affect the degeneration of supergenes. Finally, we discuss implications of the evolution of supergene haplotypes for the long-term fate of balanced polymorphisms governed by supergenes.

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Citations
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Journal ArticleDOI
TL;DR: This article investigated the origin and maintenance of four megabase-scale supergenes through analysis of whole-genome-sequencing data, including a new long-read-based genome assembly for a non-migratory Atlantic cod individual.
Abstract: Abstract Supergenes are sets of genes that are inherited as a single marker and encode complex phenotypes through their joint action. They are identified in an increasing number of organisms, yet their origins and evolution remain enigmatic. In Atlantic cod, four megabase-scale supergenes have been identified and linked to migratory lifestyle and environmental adaptations. Here we investigate the origin and maintenance of these four supergenes through analysis of whole-genome-sequencing data, including a new long-read-based genome assembly for a non-migratory Atlantic cod individual. We corroborate the finding that chromosomal inversions underlie all four supergenes, and we show that they originated at different times between 0.40 and 1.66 million years ago. We reveal gene flux between supergene haplotypes where migratory and stationary Atlantic cod co-occur and conclude that this gene flux is driven by gene conversion, on the basis of an increase in GC content in exchanged sites. Additionally, we find evidence for double crossover between supergene haplotypes, leading to the exchange of an ~275 kilobase fragment with genes potentially involved in adaptation to low salinity in the Baltic Sea. Our results suggest that supergenes can be maintained over long timescales in the same way as hybridizing species, through the selective purging of introduced genetic variation.

40 citations

Journal ArticleDOI
TL;DR: This paper investigated the origin and maintenance of four megabase-scale supergenes through analysis of whole-genome-sequencing data, including a new long-read-based genome assembly for a non-migratory Atlantic cod individual.
Abstract: Abstract Supergenes are sets of genes that are inherited as a single marker and encode complex phenotypes through their joint action. They are identified in an increasing number of organisms, yet their origins and evolution remain enigmatic. In Atlantic cod, four megabase-scale supergenes have been identified and linked to migratory lifestyle and environmental adaptations. Here we investigate the origin and maintenance of these four supergenes through analysis of whole-genome-sequencing data, including a new long-read-based genome assembly for a non-migratory Atlantic cod individual. We corroborate the finding that chromosomal inversions underlie all four supergenes, and we show that they originated at different times between 0.40 and 1.66 million years ago. We reveal gene flux between supergene haplotypes where migratory and stationary Atlantic cod co-occur and conclude that this gene flux is driven by gene conversion, on the basis of an increase in GC content in exchanged sites. Additionally, we find evidence for double crossover between supergene haplotypes, leading to the exchange of an ~275 kilobase fragment with genes potentially involved in adaptation to low salinity in the Baltic Sea. Our results suggest that supergenes can be maintained over long timescales in the same way as hybridizing species, through the selective purging of introduced genetic variation.

35 citations

Journal ArticleDOI
TL;DR: Acanthis et al. as mentioned in this paper used genome sequences to investigate the genetic basis of phenotypic variation in redpoll finches and found that variation in the redpoll phenotype is broadly controlled by a ~55-Mb chromosomal inversion.
Abstract: The genetic architecture of a phenotype can have considerable effects on the evolution of a trait or species. Characterizing genetic architecture provides insight into the complexity of a given phenotype and, potentially, the role of the phenotype in evolutionary processes like speciation. We use genome sequences to investigate the genetic basis of phenotypic variation in redpoll finches (Acanthis spp.). We demonstrate that variation in redpoll phenotype is broadly controlled by a ~55-Mb chromosomal inversion. Within this inversion, we find multiple candidate genes related to melanogenesis, carotenoid coloration, and bill shape, suggesting the inversion acts as a supergene controlling multiple linked traits. A latitudinal gradient in ecotype distribution suggests supergene driven variation in color and bill morphology are likely under environmental selection, maintaining supergene haplotypes as a balanced polymorphism. Our results provide a mechanism for the maintenance of ecotype variation in redpolls despite a genome largely homogenized by gene flow. Trait genetic architecture influences how populations evolve and adapt. Genomic analysis finds that an inversion links genetic variation controlling redpoll finch color and bill shape, allowing the maintenance of latitudinal ecotypes despite a genome largely homogenized by gene flow.

17 citations

Journal ArticleDOI
TL;DR: The present study presents the first chromosome-scale genome assembly of any heterostylous species, that of Primula veris (cowslip), and demonstrates that the S-locus evolved via multiple, asynchronous gene duplications and independent gene translocations.
Abstract: Abstract Supergenes are nonrecombining genomic regions ensuring the coinheritance of multiple, coadapted genes. Despite the importance of supergenes in adaptation, little is known on how they originate. A classic example of supergene is the S locus controlling heterostyly, a floral heteromorphism occurring in 28 angiosperm families. In Primula, heterostyly is characterized by the cooccurrence of two complementary, self-incompatible floral morphs and is controlled by five genes clustered in the hemizygous, ca. 300-kb S locus. Here, we present the first chromosome-scale genome assembly of any heterostylous species, that of Primula veris (cowslip). By leveraging the high contiguity of the P. veris assembly and comparative genomic analyses, we demonstrated that the S-locus evolved via multiple, asynchronous gene duplications and independent gene translocations. Furthermore, we discovered a new whole-genome duplication in Ericales that is specific to the Primula lineage. We also propose a mechanism for the origin of S-locus hemizygosity via nonhomologous recombination involving the newly discovered two pairs of CFB genes flanking the S locus. Finally, we detected only weak signatures of degeneration in the S locus, as predicted for hemizygous supergenes. The present study provides a useful resource for future research addressing key questions on the evolution of supergenes in general and the S locus in particular: How do supergenes arise? What is the role of genome architecture in the evolution of complex adaptations? Is the molecular architecture of heterostyly supergenes across angiosperms similar to that of Primula?

16 citations

Journal ArticleDOI
TL;DR: In this paper , the first chromosome-scale genome assembly of any heterostylous species, that of Primula veris (cowslip), was presented, and the authors demonstrated that the S-locus evolved via multiple, asynchronous gene duplications and independent gene translocations.
Abstract: Supergenes are nonrecombining genomic regions ensuring the coinheritance of multiple, coadapted genes. Despite the importance of supergenes in adaptation, little is known on how they originate. A classic example of supergene is the S locus controlling heterostyly, a floral heteromorphism occurring in 28 angiosperm families. In Primula, heterostyly is characterized by the cooccurrence of two complementary, self-incompatible floral morphs and is controlled by five genes clustered in the hemizygous, ca. 300-kb S locus. Here, we present the first chromosome-scale genome assembly of any heterostylous species, that of Primula veris (cowslip). By leveraging the high contiguity of the P. veris assembly and comparative genomic analyses, we demonstrated that the S-locus evolved via multiple, asynchronous gene duplications and independent gene translocations. Furthermore, we discovered a new whole-genome duplication in Ericales that is specific to the Primula lineage. We also propose a mechanism for the origin of S-locus hemizygosity via nonhomologous recombination involving the newly discovered two pairs of CFB genes flanking the S locus. Finally, we detected only weak signatures of degeneration in the S locus, as predicted for hemizygous supergenes. The present study provides a useful resource for future research addressing key questions on the evolution of supergenes in general and the S locus in particular: How do supergenes arise? What is the role of genome architecture in the evolution of complex adaptations? Is the molecular architecture of heterostyly supergenes across angiosperms similar to that of Primula?

15 citations

References
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Book
01 Jan 1930

14,612 citations

Journal ArticleDOI
09 Oct 2009-Science
TL;DR: Hi-C is described, a method that probes the three-dimensional architecture of whole genomes by coupling proximity-based ligation with massively parallel sequencing and demonstrates the power of Hi-C to map the dynamic conformations of entire genomes.
Abstract: We describe Hi-C, a method that probes the three-dimensional architecture of whole genomes by coupling proximity-based ligation with massively parallel sequencing. We constructed spatial proximity maps of the human genome with Hi-C at a resolution of 1 megabase. These maps confirm the presence of chromosome territories and the spatial proximity of small, gene-rich chromosomes. We identified an additional level of genome organization that is characterized by the spatial segregation of open and closed chromatin to form two genome-wide compartments. At the megabase scale, the chromatin conformation is consistent with a fractal globule, a knot-free, polymer conformation that enables maximally dense packing while preserving the ability to easily fold and unfold any genomic locus. The fractal globule is distinct from the more commonly used globular equilibrium model. Our results demonstrate the power of Hi-C to map the dynamic conformations of whole genomes.

7,180 citations

Journal ArticleDOI
TL;DR: If the selective coefficients at the linked locus are small compared to those at the substituted locus, it is shown that the probability of complete fixation at the links is approximately exp (− Nc), where c is the recombinant fraction and N the population size.
Abstract: SUMMARY When a selectively favourable gene substitution occurs in a population, changes in gene frequencies will occur at closely linked loci. In the case of a neutral polymorphism, average heterozygosity will be reduced to an extent which varies with distance from the substituted locus. The aggregate eifect of substitution on neutral polymorphism is estimated; in populations of total size 10 6 or more (and perhaps of 10 4 or more), this eifect will be more important than that of random fixation. This may explain why the extent of polymorphism in natural populations does not vary as much as one would expect from a consideration of the equilibrium between mutation and random fixation in populations of different sizes. For a selectively maintained polymorphism at a linked locus, this process will only be important in the long run if it leads to complete fixation. If the selective coefficients at the linked locus are small compared to those at the substituted locus, it is shown that the probability of complete fixation at the linked locus is approximately exp (— Nc), where c is the recombinant fraction and N the population size. It follows that in a large population a selective substitution can occur in a cistron without eliminating a selectively maintained polymorphism in the same cistron.

2,726 citations

Journal ArticleDOI
TL;DR: It is shown that this calculation does not apply for mutant genes that act advantageously only when in some special combinations with one or more other mutant genes, and that as far as these cases of special synergism are concerned recombining lines have no evolutionary advantage over non-recombining ones.
Abstract: The method of calculation is shown wherebt a formula has been derived that approximately the ratio of the rate of accumulation of advantageous mutant genes in a population that undergoes recombination to the rate in an otherwise non-recombining one. A table is given showing the ratios thus found for different frequencies of advantageous mutations and different degrees of their advantage. It is shown that this calculation does not apply for mutant genes that act advantageously only when in some special combinations with one or more other mutant genes, and that as far as these cases of special synergism are concerned recombining lines have no evolutionary advantage over non-recombining ones. Other limitations of the formula are pointed out and assessed. It is explained that most factors that retard the rate of recombination—for expample, linkage, rarity of outbreeding, intercalation of sexual reproduction between more frequent cycles of sexual propagation, and partial isolation between subpopulations—must usually cause little long-term retardation of the speed of advance that is fostered by recombination. Moreover, even where long-term evolutions has virtually ceased, recombination of mutant genes still confers upon a population the means of adopting short-term genetic “dodges”, that adjust it to ecological and “physical” changes in its circumstances, much more rapidly than would be possible for a comparable asexual population. Under conditions where only stability of type is needed, a non-recombining does not actually degenerate as a result of an excess of mutation over selection, after the usual equilibrium between these pressures is reached. However, a irreversible ratchet mechanism exists in the non-recombining species (unlike the recombining ones) that prevents selection, even if intensified, from reducing the mutational loads below the lightest that were in existence when the intensified selection started, whereas, contrariwise, “drift”, and what might be called “selective noise” must allow occasional slips of the lightest loads in the direction of increased weight.

2,240 citations

Journal ArticleDOI
01 Aug 1993-Genetics
TL;DR: Observed reductions in molecular variation in low recombination genomic regions of sufficiently large size, for instance in the centromere-proximal regions of Drosophila autosomes or in highly selfing plant populations, may be partly due to background selection against deleterious mutations.
Abstract: Selection against deleterious alleles maintained by mutation may cause a reduction in the amount of genetic variability at linked neutral sites. This is because a new neutral variant can only remain in a large population for a long period of time if it is maintained in gametes that are free of deleterious alleles, and hence are not destined for rapid elimination from the population by selection. Approximate formulas are derived for the reduction below classical neutral values resulting from such background selection against deleterious mutations, for the mean times to fixation and loss of new mutations, nucleotide site diversity, and number of segregating sites. These formulas apply to random-mating populations with no genetic recombination, and to populations reproducing exclusively asexually or by self-fertilization. For a given selection regime and mating system, the reduction is an exponential function of the total mutation rate to deleterious mutations for the section of the genome involved. Simulations show that the effect decreases rapidly with increasing recombination frequency or rate of outcrossing. The mean time to loss of new neutral mutations and the total number of segregating neutral sites are less sensitive to background selection than the other statistics, unless the population size is of the order of a hundred thousand or more. The stationary distribution of allele frequencies at the neutral sites is correspondingly skewed in favor of rare alleles, compared with the classical neutral result. Observed reductions in molecular variation in low recombination genomic regions of sufficiently large size, for instance in the centromere-proximal regions of Drosophila autosomes or in highly selfing plant populations, may be partly due to background selection against deleterious mutations.

1,807 citations