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An ancient recombination desert is a speciation supergene in placental mammals

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Abstract

Gene flow between biological species is a common and often adaptive evolutionary phenomenon throughout the tree of life1,2,3,4. Given the pervasive nature of genetic exchange, a daunting challenge is how best to infer the correct relationships between species from the complex collection of histories arrayed across genomes5. The local rate of meiotic recombination influences the distribution of signatures of, and barriers to, gene flow during the early stages of speciation6. Still, a broader understanding of this relationship and its application to accurately discerning phylogeny is lacking due to a scarcity of recombination maps. Here we applied deep learning methods to genome alignments from 22 divergent placental mammal species to infer the evolution of the recombination landscape. We identified a large and evolutionarily conserved X-linked recombination desert constituting 30% of the chromosome. Recombination-aware phylogenomic analyses from 94 species revealed that the X-linked recombination desert is an ancient and recurrent barrier to gene flow and retains the species history when introgression dominates genome-wide ancestry. The functional basis for this supergene is manifold, enriched with genes that influence sex chromosome silencing and reproduction traits. Because the locus underpins reproductive isolation across ordinal lineages, it may represent a reliable marker for resolving challenging relationships across the mammalian phylogeny.

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Fig. 1: Comparative dataset for recombination-aware phylogenomics.
Fig. 2: Evolutionary conservation of synteny, linkage and recombination patterns across the placental mammal phylogeny.
Fig. 3: Species-tree frequency is highest in genomic regions with low recombination rates and in the XLRD.
Fig. 4: Genome-wide ancestry distribution patterns.
Fig. 5: XLRD restricted gene flow is reflected in population genomic data.

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Data availability

All publicly available data used as part of this study are listed in the relevant tables. New Illumina short-read sequencing data have been submitted to NCBI’s short-read archive and are available under bioproject IDsPRJNA1333566 andPRJNA1335549. Recombination maps and.vcf files are available at Zenodo (https://doi.org/10.5281/zenodo.15131984)93.

Code availability

Existing software used as part of the analyses is referenced in the main text. Custom scripts associated with the analyses are available at GitHub (https://github.com/eutherialab/Foley_XLRD).

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Acknowledgements

We would like to acknowledge the undergraduate researchers who participated in Aggie Research Teams during this project: S. Archard, M. Clark, S. Gaikaiwari and J. Arukakkal. We also thank A. Camagnini, L. Frantz and G. Larson for providing a published version of a variant call file ofFelis species. Portions of this research were conducted with the advanced computing resources provided by Texas A&M High-Performance Research Computing. This work was funded by National Science Foundation grants DEB-1753760, awarded to W.J.M., and DEB-2150664, awarded to W.J.M. and T.R. The black-footed ferret data were funded by a Morris Animal Foundation grant, D18ZO-058, awarded to K.P.K.

Author information

Authors and Affiliations

  1. Veterinary Integrative Biosciences, Texas A&M University, College Station, TX, USA

    Nicole M. Foley, Richard G. Rasulis, Zoya Wani, Mayra N. Mendoza Cerna, Terje Raudsepp & William J. Murphy

  2. Interdisciplinary Program in Genetics and Genomics, Texas A&M University, College Station, TX, USA

    Mayra N. Mendoza Cerna, Terje Raudsepp & William J. Murphy

  3. Smithsonian-Mason School of Conservation, George Mason University, Front Royal, VA, USA

    Henrique V. Figueiró & Klaus Peter Koepfli

Authors
  1. Nicole M. Foley
  2. Richard G. Rasulis
  3. Zoya Wani
  4. Mayra N. Mendoza Cerna
  5. Henrique V. Figueiró
  6. Klaus Peter Koepfli
  7. Terje Raudsepp
  8. William J. Murphy

Contributions

W.J.M. and N.M.F. conceived and designed the project. W.J.M., T.R. and N.M.F. supervised the project. Recombination maps were created by N.M.F., R.G.R., Z.W. and M.N.M.C. Comparative recombination analyses were carried out by N.M.F.Mustela nigripes population genomic data were supplied by H.V.F. and K.P.K. Phylogenomic, population genomic and functional analyses were conducted by N.M.F. The paper was authored by W.J.M. and N.M.F. with contributions from all authors. All authors reviewed and approved the final manuscript.

Corresponding authors

Correspondence toNicole M. Foley orWilliam J. Murphy.

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Competing interests

The authors declare no competing interests.

Peer review

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Nature thanks the anonymous reviewer(s) for their contribution to the peer review of this work.Peer reviewer reports are available.

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Extended data figures and tables

Extended Data Fig. 1 Comparison of recombination maps using parent-offspring trio-inferred versus pan-mammal mutation rates.

a,Macaca mulatta (n = 4: individuals) maps inferred with both rates showed a significant correlation (Spearman’s rho = 0.75,p < 2.2e-16; Kendall’s tau = 0.55,p < 2.2e-16, z = 44.972).b,Papio anubis (n = 3: individuals) maps inferred with both rates also showed a significant correlation (Spearman’s rho = 0.80,p < 2.2e-16; Kendall’s tau = 0.61,p < 2.2e-16, z = 47.838).

Extended Data Fig. 2 The effect of population substructure on estimating recombination rates along the X chromosome.

PCA of three data subsets (colors), with varying numbers of individuals shown in the PCA forMacaca mulatta. All samples were submitted to SRA by Oregon Health and Science University. Statistical analysis focused on the extremes of the dataset comparisons; N-12 vs N = 4, and the indicated recombination landscapes were significantly correlated (Spearman’s rho = 0.74,p < 2.2e-16) (Kendall’s tau = 0.56,p < 2.2e-16, z = 44.587).

Extended Data Fig. 3 Comparison of ReLERNN recombination maps for the X chromosome with multigenerational pedigree-based linkage maps.

a, The ReLERNN map generated forSus scrofa closely resembles the landscape shown in pedigree-based recombination maps35.b, Comparison of recombination maps for the domestic cat X chromosome based on linkage analysis of multigenerational pedigrees94 (blue) and a domestic cat ReLERNN map derived from 10 (orange) and 3 (green) individuals of the Persian cat breed.

Extended Data Fig. 4 The recombination landscape of the X chromosome is conserved among closely related species.

a, Conservation of the recombination landscape between subspecies ofPanthera tigris (P. t. jacksoni n = 4: individuals;P.t. sumatrae n = 4: individuals) (Spearman’s rho = 0.78,p < 2.2e-16) (Kendall’s tau = 0.60,p < 2.2e-16, z = 38.719).b, Conservation of the recombination landscape between closely related dolphin species,Tursiops truncatus (n = 4: individuals) andTursiops aduncus (n = 4: individuals) (Spearman’s rho = 0.90,p < 2.2e-16) (Kendall’s tau = 0.72,p < 2.2e-16, z = 54.865).

Extended Data Fig. 5 Nucleotide diversity and effective population size across a subset of species for which we generated a recombination map.

a, There was no systematic difference between primates derived from captive populations used for research purposes and the rest of the wild and domestic species in terms of nucleotide diversity and effective population size. Estimates of effective population sizes are from Wilder et al.71. Species names in purple indicate closely related species with similar IUCN statuses.b, Despite a large difference in nucleotide diversity betweenPrionailurus bengalensis (n = 5: individuals; IUCN Least Concern) andPanthera tigris (n = 4: individuals; IUCN Endangered), a similar recombination landscape on the X chromosome was observed. These results suggest that our recombination maps are robust to differences in nucleotide diversity (Spearman’s rho = 0.81,p < 2.2e-16) (Kendall’s tau = 0.60,p < 2.2e-16, z = 39.92).

Extended Data Fig. 6 The relationship between the frequency of T1 (shown in blue – the species tree) and recombination quintiles for Group 1 and 2.

The relationship between the recombination quintiles and the next most frequent non-species topology is shown in red. Where correlations do not match the patterns observed in most species (e.g., dolphins – bottom), these clades typically show a higher level of ILS as the cause of discordance (see Supplementary Table6).

Extended Data Fig. 7 Genome-wide distribution patterns of species (blue) and introgression (red) locus trees in laurasiatherian mammals with rearranged X chromosomes.

a, Genome-wide distributions of the species tree and introgression-associated tree. Note the enrichment of the species tree on the X.b, SVbyEye76 plots detail which parts of the rearranged X chromosomes ofMyotis andBos are syntenic to the human XLRD. Despite rearrangement, regions syntenic to the human XLRD coincide with peaks of species tree frequency.

Extended Data Fig. 9 Functional components of a speciation supergene.

a, An ideogram of the human X chromosome showing the locations of major evolutionary strata in mammals: the X-added region, and the X-conserved region. The positions of X chromosome inactivation (XCI; female-specific) and meiotic sex chromosome inactivation (MSCI; male-specific) expressed components are indicated below the ideogram43. The locations of significant loci from a male-specific testosterone GWAS are shown relative to the XLRD. The distribution and density of genes associated with ovary- and testis-biased gene expression are also displayed relative to the XLRD. Genes with biased expression in the ovaries are significantly enriched inside of the XLRD (chi-squared = 3.92,p-value = 0.048). Ampliconic genes are clustered within the XLRD compared to the whole X chromosome: a, human (53%),b, cat (87%), and pig (79%). Testis-specific ampliconic genes in cats (chi-squared = 36.11,p-value < 0.00001) and pigs (chi-squared = 19.66,p-value < 0.00001) are significantly enriched in the XLRD at α = 0.05.

Extended Data Table 1 Previous phylogenomic and population genomic studies that identified introgression

Supplementary information

Supplementary Information

Supplementary Figs. 1–42 and Tables 1–10.

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Foley, N.M., Rasulis, R.G., Wani, Z.et al. An ancient recombination desert is a speciation supergene in placental mammals.Nature (2025). https://doi.org/10.1038/s41586-025-09740-2

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