Dynamic molecular evolution of a supergene with suppressed recombination in white-throated sparrows

  1. Hyeonsoo Jeong
  2. Nicole M Baran
  3. Dan Sun
  4. Paramita Chatterjee
  5. Thomas S Layman
  6. Christopher N Balakrishnan
  7. Donna L Maney
  8. Soojin V Yi

  • Curated by eLife

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    Evaluation Summary:

    In this paper, the authors generate and analyze new genome and gene expression data to understand better the evolution of the white-throated sparrow supergene region, which contains 1000 genes and determines whether a bird has a tan or a white stripe. The study nicely illustrates how the cessation of recombination that results from a chromosomal inversion can become a source of evolutionary novelty. The lack of recombination can result in the accumulation of deleterious variation leading to degeneration, but it can also (as here) facilitate genomic diversification and adaptation. The results will be of interest to a broad array of researchers studying genome architecture and phenotypic diversity and evolution.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)

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Abstract

In white-throated sparrows, two alternative morphs differing in plumage and behavior segregate with a large chromosomal rearrangement. As with sex chromosomes such as the mammalian Y, the rearranged version of chromosome two (ZAL2 m ) is in a near-constant state of heterozygosity, offering opportunities to investigate both degenerative and selective processes during the early evolutionary stages of ‘supergenes.’ Here, we generated, synthesized, and analyzed extensive genome-scale data to better understand the forces shaping the evolution of the ZAL2 and ZAL2 m chromosomes in this species. We found that features of ZAL2 m are consistent with substantially reduced recombination and low levels of degeneration. We also found evidence that selective sweeps took place both on ZAL2 m and its standard counterpart, ZAL2, after the rearrangement event. Signatures of positive selection were associated with allelic bias in gene expression, suggesting that antagonistic selection has operated on gene regulation. Finally, we discovered a region exhibiting long-range haplotypes inside the rearrangement on ZAL2 m . These haplotypes appear to have been maintained by balancing selection, retaining genetic diversity within the supergene. Together, our analyses illuminate mechanisms contributing to the evolution of a young chromosomal polymorphism, revealing complex selective processes acting concurrently with genetic degeneration to drive the evolution of supergenes.

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  1. Version published to 10.7554/elife.79387 on eLife
  2. eLife

    Author Response

    Reviewer #2 (Public Review):

    This is a nice study that pulls together a new reference genome and several levels of new popgen and RNAseq data and new analyses to provide interesting new insight on some of the evolutionary forces affecting the evolution of the ~Zal2/Zal2m system which underpins the stripe-colour polymorphism in the white-throated sparrow. The data are well balanced between homozygous Zal2/Zal2 and heterozygous Zal2m/Zal2m birds, and at a technical level, the authors do a good job of accounting for difficulties in disentangling the Zal2 and Zal2m chromosomes in heterozygous birds.

    The authors convincingly show that Zal2m has signs of degeneration, similarly to what has been shown in the fire ant Sb supergene and young Y chromosomes. They show this using multiple approaches (increase in repetitive elements, reduced genetic diversity, increased non-synonymous substitutions...). But they also show that part of Zal2m (which is rare in homozygous form) has something interesting going on, with higher local diversity and evidence of balancing selection. Analysis of allelic-biased expression shows signatures of degeneration, but also that allelic bias is associated with expression differences between morphs.

    The paper is generally well written and includes much novel insight on a timely topic and system.

    Weaknesses in this study might come from:

    • Not fully considering differences in the effects of repetitive elements on apparent genotypes (e.g, segmental duplications or jumping of repetitive elements which may have occurred in Zal2m and which lead reads to appear to be somewhere they are not).
    • Difficulties in accounting for variation in recombination rates along the genome, where low recombination can lead to patterns that look like selective sweeps.
    • Some ambiguities in interpreting allelic biases as adaptive where many of them can simply be collateral effects of the supergene architecture.

    Many of the patterns seen and interpretations offered are similar to what is known from young sex chromosomes, such as in Drosophila, but also the anther rust mating type loci and the fire ant Sb social supergene. The haploid systems of anther rust fungus and fire ant males are able to examine such patterns in more depth than what is readily accessible here.

    We appreciate an overall balanced perspective on our work. We addressed the specific concerns. Some of the limitations of the current system include the lack of high quality long-range sequence data from the species, thus making it difficult to resolve structural variation and repetitive sequences.

  3. eLife

    Evaluation Summary:

    In this paper, the authors generate and analyze new genome and gene expression data to understand better the evolution of the white-throated sparrow supergene region, which contains 1000 genes and determines whether a bird has a tan or a white stripe. The study nicely illustrates how the cessation of recombination that results from a chromosomal inversion can become a source of evolutionary novelty. The lack of recombination can result in the accumulation of deleterious variation leading to degeneration, but it can also (as here) facilitate genomic diversification and adaptation. The results will be of interest to a broad array of researchers studying genome architecture and phenotypic diversity and evolution.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)

  4. eLife

    Reviewer #1 (Public Review):

    Jeong and collaborators study the genomic evolution of a supergene that is very well documented in the literature. This supergene derives from an inversion that affects more than 100Mb of the genome of white-throated sparrows. This supergene has resulted from a chromosomal inversion that makes recombination very difficult. As a result of the lack of recombination, mutational changes in the inverted sequences can accumulate leading to the accumulation of deleterious variants and structural changes. This is likely to lead to the degeneration of the chromosome, as has taken place in the sexual chromosomes of birds and mammals. The study of such a large inversion that occurred relatively recently offers a great opportunity to investigate the early stages of chromosomal degeneration. However, the relaxation of selective forces that result from the small effective population size associated with the inversion facilitates the accumulation of genetic variation, that can contribute to genetic divergence and adaptation.

    The study of these two effects associated with the inversion makes this study very unique and this is combined with the use of high-quality genomic data for many individuals and very diverse analytical tools.

    The authors first analyze chromosomal degeneration by combining data on the number of scaffolds generated for a deeply sequenced super-white bird (ZAL2m homozygote), assessing the relative frequency of insertions and deletions, estimating the ratio of non-synonymous to synonymous fixed differences, etc. All these lines of evidence very convincingly show a certain degree of degeneration of the chromosome carrying the inversion.

    Selective forces acting on the inverted chromosome and its counterpart are then analyzed in detail including the study of the chromosomal sequences and gene expression in different tissues. The results show differences in the expression of alleles from each of the two chromosomal variants and reveal the presence of a smaller region within the inversion where divergent alleles are maintained by balancing selection, selective sweeps, and positive selection for some alleles. Although these results are very well supported in most cases, the results relative to differences in expression of specific genes need to be further investigated. Since many genes are potentially studied at the same time, it is important to further investigate possible false positives. Similarly, the detailed study of phenotypic effects requires in-depth analyses of many more individuals and with statistical designs that take into account the effect of covariates and multiple testing.

  5. eLife

    Reviewer #2 (Public Review):

    This is a nice study that pulls together a new reference genome and several levels of new popgen and RNAseq data and new analyses to provide interesting new insight on some of the evolutionary forces affecting the evolution of the ~Zal2/Zal2m system which underpins the stripe-colour polymorphism in the white-throated sparrow. The data are well balanced between homozygous Zal2/Zal2 and heterozygous Zal2m/Zal2m birds, and at a technical level, the authors do a good job of accounting for difficulties in disentangling the Zal2 and Zal2m chromosomes in heterozygous birds.

    The authors convincingly show that Zal2m has signs of degeneration, similarly to what has been shown in the fire ant Sb supergene and young Y chromosomes. They show this using multiple approaches (increase in repetitive elements, reduced genetic diversity, increased non-synonymous substitutions...). But they also show that part of Zal2m (which is rare in homozygous form) has something interesting going on, with higher local diversity and evidence of balancing selection. Analysis of allelic-biased expression shows signatures of degeneration, but also that allelic bias is associated with expression differences between morphs.

    The paper is generally well written and includes much novel insight on a timely topic and system.

    Weaknesses in this study might come from:
    - Not fully considering differences in the effects of repetitive elements on apparent genotypes (e.g, segmental duplications or jumping of repetitive elements which may have occurred in Zal2m and which lead reads to appear to be somewhere they are not).
    - Difficulties in accounting for variation in recombination rates along the genome, where low recombination can lead to patterns that look like selective sweeps.
    - Some ambiguities in interpreting allelic biases as adaptive where many of them can simply be collateral effects of the supergene architecture.

    Many of the patterns seen and interpretations offered are similar to what is known from young sex chromosomes, such as in Drosophila, but also the anther rust mating type loci and the fire ant Sb social supergene. The haploid systems of another rust fungus and fire ant males are able to examine such patterns in more depth than what is readily accessible here.

  6. Version published to 10.1101/2022.02.28.481145v2 on bioRxiv
  7. Version published to 10.1101/2022.02.28.481145v1 on bioRxiv