Skip to main content

Thank you for visiting nature.com. 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). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Extreme Y chromosome polymorphism corresponds to five male reproductive morphs of a freshwater fish

Nature Ecology & Evolution volume 5, pages 939–948 (2021)Cite this article

Subjects

Abstract

Loss of recombination between sex chromosomes often depletes Y chromosomes of functional content and genetic variation, which might limit their potential to generate adaptive diversity. Males of the freshwater fish Poecilia parae occur as one of five discrete morphs, all of which shoal together in natural populations where morph frequency has been stable for over 50 years. Each morph uses a different complex reproductive strategy and morphs differ dramatically in colour, body size and mating behaviour. Morph phenotype is passed perfectly from father to son, indicating there are five Y haplotypes segregating in the species, which encode the complex male morph characteristics. Here, we examine Y diversity in natural populations of P. parae. Using linked-read sequencing on multiple P. parae females and males of all five morphs, we find that the genetic architecture of the male morphs evolved on the Y chromosome after recombination suppression had occurred with the X. Comparing Y chromosomes between each of the morphs, we show that, although the Ys of the three minor morphs that differ in colour are highly similar, there are substantial amounts of unique genetic material and divergence between the Ys of the three major morphs that differ in reproductive strategy, body size and mating behaviour. Altogether, our results suggest that the Y chromosome is able to overcome the constraints of recombination loss to generate extreme diversity, resulting in five discrete Y chromosomes that control complex reproductive strategies.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Coverage differences between the sexes (male:female log2) for female scaffolds placed by RACA on the reference Xiphophorus hellerii chromosomes.
Fig. 2: Bayesian Y chromosome phylogeny based on presence/absence of the 27,950,090 P. parae Y-mers and 1,646 P. picta Y-mers25 in each individual and rooted on P. picta.
Fig. 3: The distribution of the 27,950,090 P. parae Y-mers reveals strong differences across morphs.
Fig. 4: Comparison of mapping coverage for scaffolds enriched with melanzona, immaculata and parae morph-mers.

Data availability

All of the data generated for this study have been made available in the NCBI repository under the BioProject accession number PRJNA714257.

Code availability

All scripts and pipelines for analyses are available at https://github.com/manklab/Poecilia_parae_Y_Diversity

References

  1. Bachtrog, D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 14, 113–124 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Tobler, R., Nolte, V. & Schlotterer, C. High rate of translocation-based gene birth on the Drosophila Y chromosome. Proc. Natl Acad. Sci. USA 114, 11721–11726 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Mahajan, S. & Bachtrog, D. Convergent evolution of Y chromosome gene content in flies. Nat. Commun. 8, 785 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bachtrog, D., Mahajan, S. & Bracewell, R. Massive gene amplification on a recently formed Drosophila Y chromosome. Nat. Ecol. Evol. 3, 1587–1597 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Hall, A. B. et al. Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes. Proc. Natl Acad. Sci. USA 113, E2114–E2123 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Todesco, M. et al. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature 584, 602–607 (2020).

    Article  CAS  PubMed  Google Scholar 

  7. Schwander, T., Libbrecht, R. & Keller, L. Supergenes and complex phenotypes. Curr. Biol. 24, 288–294 (2014).

    Article  Google Scholar 

  8. Wang, J. et al. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493, 664–668 (2013).

    Article  CAS  PubMed  Google Scholar 

  9. Lamichhaney, S. et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat. Genet. 48, 84–88 (2016).

    Article  CAS  PubMed  Google Scholar 

  10. Kupper, C. et al. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet. 48, 79–83 (2016).

    Article  CAS  PubMed  Google Scholar 

  11. Branco, S. et al. Multiple convergent supergene evolution events in mating-type chromosomes. Nat. Commun. 9, 2000 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Yan, Z. et al. Evolution of a supergene that regulates a trans-species social polymorphism. Nat. Ecol. Evol. 4, 240–249 (2020).

    Article  PubMed  Google Scholar 

  13. Lindholm, A. K., Brooks, R. & Breden, F. Extreme polymorphism in a Y-linked sexually selected trait. Heredity 92, 156–162 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Hurtado-Gonzales, J. L. & Uy, J. A. Alternative mating strategies may favour the persistence of a genetically based colour polymorphism in a pentamorphic fish. Anim. Behav. 77, 1187–1194 (2009).

    Article  Google Scholar 

  15. Hurtado-Gonzales, J. L. & Uy, J. A. Intrasexual competition facilitates the evolution of alternative mating strategies in a colour polymorphic fish. BMC Evol. Biol. 10, 391 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hurtado-Gonzales, J. L., Baldassarre, D. T. & Uy, J. A. Interaction between female mating preferences and predation may explain the maintenance of rare males in the pentamorphic fish Poecilia parae. J. Evol. Biol. 23, 1293–1301 (2010).

    Article  PubMed  Google Scholar 

  17. Hurtado-Gonzales, J. L., Loew, E. R. & Uy, J. A. Variation in the visual habitat may mediate the maintenance of color polymorphism in a poeciliid fish. PLoS ONE 9, e101497 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Sandkam, B. A., Young, C. M., Breden, F. M., Bourne, G. R. & Breden, F. Color vision varies more among populations than among species of live-bearing fish from South America. BMC Evol. Biol. 15, 225 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Bourne, G. R., Breden, F. & Allen, T. C. Females prefer carotenoid colored males as mates in the pentamorphic livebearing fish, Poecilia parae. Naturwissenschaften 90, 402–405 (2003).

    Article  CAS  PubMed  Google Scholar 

  20. Liley, N. R. Reproductive Isolation in Some Sympatric Species of Fishes. PhD thesis, Oxford Univ. (1963).

  21. Bachtrog, D. et al. Are all sex chromosomes created equal? Trends Genet. 27, 350–357 (2011).

    Article  CAS  PubMed  Google Scholar 

  22. Rice, W. R. Evolution of the Y sex chromosome in animals. BioScience 46, 331–343 (1996).

    Article  Google Scholar 

  23. Wright, A. E., Dean, R., Zimmer, F. & Mank, J. E. How to make a sex chromosome. Nat. Commun. 7, 12087 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Furman, B. L. S. et al. Sex chromosome evolution: so many exceptions to the rules. Genome Biol. Evol. 12, 750–763 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Darolti, I. et al. Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers. Proc. Natl Acad. Sci. USA 116, 19031–19036 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Wright, A. et al. Convergent recombination suppression suggests a role of sexual selection in guppy sex chromosome formation. Nat. Commun. 8, 14251 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Darolti, I., Wright, A. E. & Mank, J. E. Guppy Y chromosome integrity maintained by incomplete recombination suppression. Genome Biol. Evol. 12, 965–977 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Almeida, P. et al. Divergence and remarkable diversity of the Y chromosome in guppies. Mol. Biol. Evol. 38, 619–633 (2021).

    Article  PubMed  Google Scholar 

  29. Rabosky, D. L. et al. An inverse latitudinal gradient in speciation rate for marine fishes. Nature 559, 392–395 (2018).

    Article  CAS  PubMed  Google Scholar 

  30. Reznick, D. N., Miles, D. B. & Winslow, S. Life history of Poecilia picta (Poeciliidae) from the Island of Trinidad. Copeia 1992, 782–790 (1992).

    Article  Google Scholar 

  31. Haskins, C. P. & Haskins, E. F. The role of sexual selection as an isolating mechanism in three species of poeciliid fishes. Evolution 3, 160–169 (1949).

    Article  CAS  PubMed  Google Scholar 

  32. Liley, N. R. Ethological isolating mechanisms in four sympatric species of poeciliid fishes. Behav. Suppl. 14, 1–197 (1966).

    Google Scholar 

  33. Vicoso, B. & Bachtrog, D. Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature 499, 332–335 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Vicoso, B. & Bachtrog, D. Numerous transitions of sex chromosomes in Diptera. PLoS Biol. 13, e1002078 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Vicoso, B., Emerson, J. J., Zektser, Y., Mahajan, S. & Bachtrog, D. Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol. 11, e1001643 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kim, J. et al. Reference-assisted chromosome assembly. Proc. Natl Acad. Sci. USA 110, 1785–1790 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Pucholt, P., Wright, A. E., Conze, L. L., Mank, J. E. & Berlin, S. Recent sex chromosome divergence despite ancient dioecy in the willow Salix viminalis. Mol. Biol. Evol. 34, 1991–2001 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Akagi, T., Henry, I. M., Tao, R. & Comai, L. A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons. Science 346, 646–650 (2014).

    Article  CAS  PubMed  Google Scholar 

  39. Torres, M. F. et al. Genus-wide sequencing supports a two-locus model for sex-determination in Phoenix. Nat. Commun. 9, 3969 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Morris, J., Darolti, I., Bloch, N. I., Wright, A. E. & Mank, J. E. Shared and species-specific patterns of nascent Y chromosome evolution in two guppy species. Genes 9, 238 (2018).

    Article  PubMed Central  Google Scholar 

  41. Napolitano, L. M. & Meroni, G. TRIM family: pleiotropy and diversification through homomultimer and heteromultimer formation. IUBMB Life 64, 64–71 (2012).

    Article  CAS  PubMed  Google Scholar 

  42. Sardiello, M., Cairo, S., Fontanella, B., Ballabio, A. & Meroni, G. Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties. BMC Evol. Biol. 8, 225 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Karki, R. et al. NLRC3 is an inhibitory sensor of PI3K-mTOR pathways in cancer. Nature 540, 583–587 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sandkam, B. A. et al. Tbx2a modulates switching of RH2 and LWS opsin gene expression. Mol. Biol. Evol. 37, 2002–2014 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Showell, C., Christine, K. S., Mandel, E. M. & Conlon, F. L. Developmental expression patterns of Tbx1, Tbx2, Tbx5, and Tbx20 in Xenopus tropicalis. Dev. Dyn. 235, 1623–1630 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Gibson-Brown, J. J., S, I. A., Silver, L. M. & Papaioannou, V. E. Expression of T-box genes Tbx2-Tbx5 during chick organogenesis. Mech. Dev. 74, 165–169 (1998).

    Article  CAS  PubMed  Google Scholar 

  47. Tomaszkiewicz, M., Chalopin, D., Schartl, M., Galiana, D. & Volff, J.-N. A multicopy Y-chromosomal SGNH hydrolase gene expressed in the testis of the platyfish has been captured and mobilized by a Helitron transposon. BMC Genet. 15, 44 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Smit, A. F. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr. Opin. Genet. Dev. 9, 657–663 (1999).

    Article  CAS  PubMed  Google Scholar 

  49. Sotero-Caio, C. G., Platt, R. N. 2nd, Suh, A. & Ray, D. A. Evolution and diversity of transposable elements in vertebrate genomes. Genome Biol. Evol. 9, 161–177 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Felsenstein, J. The evolutionary advantage of recombination. Genetics 78, 737–756 (1974).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Lenormand, T., Fyon, F., Sun, E. & Roze, D. Sex chromosome degeneration by regulatory evolution. Curr. Biol. 30, 3001–3006 (2020).

    Article  CAS  PubMed  Google Scholar 

  52. Hough, J., Wang, W., Barrett, S. C. H. & Wright, S. I. Hill–Robertson interference reduces genetic diversity on a young plant Y-chromosome. Genetics 207, 685 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Marais, G. A. et al. Evidence for degeneration of the Y chromosome in the dioecious plant Silene latifolia. Curr. Biol. 18, 545–549 (2008).

    Article  CAS  PubMed  Google Scholar 

  54. Bachtrog, D. & Charlesworth, B. Reduced adaptation of a non-recombining neo-Y chromosome. Nature 416, 323–326 (2002).

    Article  CAS  PubMed  Google Scholar 

  55. Mank, J. E. Small but mighty: the evolutionary dynamics of W and Y sex chromosomes. Chromosome Res. 20, 21–33, (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kaiser, V. B. & Charlesworth, B. Muller’s ratchet and the degeneration of the Drosophila miranda neo-Y chromosome. Genetics 185, 339–348 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Keightley, P. D. & Otto, S. P. Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443, 89–92 (2006).

    Article  CAS  PubMed  Google Scholar 

  58. Ritz, K. R., Noor, M. A. F. & Singh, N. D. Variation in recombination rate: adaptive or not? Trends Genet. 33, 364–374 (2017).

    Article  CAS  PubMed  Google Scholar 

  59. Metzger, D. C. H., Sandkam, B. A., Darolti, I. & Mank, J. E. Rapid evolution of complete dosage compensation in Poecilia. Preprint at bioRxiv https://doi.org/10.1101/2021.02.12.431036 (2021).

  60. Lemos, B., Araripe, L. O. & Hartl, D. L. Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences. Science 319, 91–93 (2008).

    Article  CAS  PubMed  Google Scholar 

  61. Ellegren, H. Characteristics, causes and evolutionary consequences of male-biased mutation. Proc. Biol. Sci. 274, 1–10 (2007).

    CAS  PubMed  Google Scholar 

  62. Tennessen, J. A. et al. Repeated translocation of a gene cassette drives sex-chromosome turnover in strawberries. PLoS Biol. 16, e2006062 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Bourque, G. et al. Ten things you should know about transposable elements. Genome Biol. 19, 199 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Carleton, K. L. et al. Movement of transposable elements contributes to cichlid diversity. Mol. Ecol. 29, 4956–4969 (2020).

    Article  CAS  PubMed  Google Scholar 

  65. Brawand, D. et al. The genomic substrate for adaptive radiation in African cichlid fish. Nature 513, 375–381 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Auvinet, J. et al. Mobilization of retrotransposons as a cause of chromosomal diversification and rapid speciation: the case for the Antarctic teleost genus Trematomus. BMC Genom. 19, 339 (2018).

    Article  CAS  Google Scholar 

  67. Naville, M. et al. Not so bad after all: retroviruses and long terminal repeat retrotransposons as a source of new genes in vertebrates. Clin. Microbiol. Infect. 22, 312–323 (2016).

    Article  CAS  PubMed  Google Scholar 

  68. Sinervo, B. & Calsbeek, R. The developmental, physiological, neural, and genetical causes and consequences of frequency-dependent selection in the wild. Annu. Rev. Ecol. Evol. Syst. 37, 581–610 (2006).

    Article  Google Scholar 

  69. Sinervo, B. & Lively, C. M. The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380, 240–243 (1996).

    Article  CAS  Google Scholar 

  70. Hartl, D. L. & Clark, A. G. Principles of Population Genetics (Sinauer Associates, 1997).

  71. Lank, D. B., Smith, C. M., Hanotte, O., Burke, T. & Cooke, F. Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax. Nature 378, 59–62 (1995).

    Article  CAS  Google Scholar 

  72. Tuttle, E. M. et al. Divergence and functional degradation of a sex chromosome-like supergene. Curr. Biol. 26, 344–350 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Hunt, B. G. Supergene evolution: recombination finds a way. Curr. Biol. 30, 73–76, (2020).

    Article  Google Scholar 

  74. Charlesworth, D. The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations. Evol. Appl. 9, 74–90 (2016).

    Article  PubMed  Google Scholar 

  75. Joron, M. et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477, 203–206 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Elyanow, R., Wu, H.-T. & Raphael, B. J. Identifying structural variants using linked-read sequencing data. Bioinformatics 34, 353–360 (2018).

    Article  CAS  PubMed  Google Scholar 

  78. Harris, R. S. Improved Pairwise Alignment of Genomic DNA. PhD thesis, Pennsylvania State Univ. (2007).

  79. Kent, W. J., Baertsch, R., Hinrichs, A., Miller, W. & Haussler, D. Evolution’s cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc. Natl Acad. Sci. USA 100, 11484–11489 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589–595 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1, 2047–217X–1–18 (2012).

  83. Palmer, D. H., Rogers, T. F., Dean, R. & Wright, A. E. How to identify sex chromosomes and their turnover. Mol. Ecol. 28, 4709–4724 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  84. Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  85. Carvalho, A. B. & Clark, A. G. Efficient identification of Y chromosome sequences in the human and Drosophila genomes. Genome Res. 23, 1894–1907 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Carvalho, A. B., Vicoso, B., Russo, C. A., Swenor, B. & Clark, A. G. Birth of a new gene on the Y chromosome of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 112, 12450–12455 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  88. Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinform. 12, 491 (2011).

  89. Smit, A., Hubley, R. RepeatModeler Open-1.0. (ISB, 2013-2015); http://www.repeatmasker.org

  90. Smit, A., Hubley, R. & Green, P. RepeatMasker Open-4.0. (ISB, 2013-2015); http://www.repeatmasker.org

  91. Howe, K. L. et al. Ensembl Genomes 2020-enabling non-vertebrate genomic research. Nucleic Acids Res. 48, D689–D695 (2020).

    Article  CAS  PubMed  Google Scholar 

  92. Dreyer, C. et al. ESTs and EST-linked polymorphisms for genetic mapping and phylogenetic reconstruction in the guppy, Poecilia reticulata. BMC Genom. 8, 269 (2007).

  93. Sharma, E. et al. Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata. BMC Genom. 15, 400 (2014).

  94. Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290–295 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Stanke, M. et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435–W439 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Seppey, M., Manni, M. & Zdobnov, E. M. in Gene Prediction (ed. Kollmar, M.) 227–245 (Humana, 2019).

  97. Korf, I. Gene finding in novel genomes. BMC Bioinform. 5, 59 (2004).

  98. Katoh, K., Asimenos, G. & Toh, H. Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537, 39–64 (2009).

    Article  CAS  PubMed  Google Scholar 

  99. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the members of the Mank lab and N. Prior for stimulating conversations and excellent feedback on early drafts of the manuscript. This was supported by the Natural Sciences and Engineering Research Council of Canada through a Banting Postdoctoral Fellowship (to B.A.S.), the European Research Council (grant nos. 260233 and 680951 to J.E.M.) and a Canada 150 Research Chair (to J.E.M.). Field work was conducted under Permit 120616 SP: 015 from the Environmental Protection Agency of Guyana. Sequencing was performed by the SNP&SEQ Technology Platform in Uppsala, Sweden. The CEIBA Biological Center partially subsidized our expenses during field collection in Guyana. We thank C. Lacy for the fish illustrations.

Author information

Authors and Affiliations

  1. Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada

    Benjamin A. Sandkam, Iulia Darolti, Benjamin L. S. Furman, Wouter van der Bijl & Judith E. Mank

  2. Department of Genetics, Evolution and Environment, University College London, London, UK

    Pedro Almeida & Jake Morris

  3. Department of Biology, University of Missouri-St. Louis, St. Louis, MO, USA

    Godfrey R. Bourne

  4. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada

    Felix Breden

Authors
  1. Benjamin A. Sandkam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pedro Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Iulia Darolti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benjamin L. S. Furman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wouter van der Bijl
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jake Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Godfrey R. Bourne
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Felix Breden
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Judith E. Mank
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

B.A.S. and J.E.M. designed the research. B.A.S., J.E.M, F.B. and G.R.B. conducted field work. B.A.S., P.A., I.D., B.L.S.F., W.v.d.B. and J.M. conducted bioinformatic analyses. B.A.S., P.A., I.D., B.L.S.F., W.v.d.B., J.M., G.R.B., F.B. and J.E.M. wrote the paper.

Corresponding author

Correspondence to Benjamin A. Sandkam.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Divergence between X and Y in Poecilia parae and the sister species Poecilia picta indicate recombination was stopped before the five morphs controlled by the Y chromosome evolved in Poecilia parae.

a, M:F log2 coverage of RACA anchored scaffolds for all five morphs of P. parae (red) and the close relative P. picta (black)25. Lines represent sliding window of 15 scaffolds. Shaded bars represent the 95% confidence interval based on bootstrapping coverage across the autosomes for P. parae (pink) and P. picta (grey). b, Phylogeny from The Fish Tree of Life29. Orange indicate species for which chr 8 is known to be the Y and is highly diverged from the X. Blue indicates species for which chr 8 is known to be not degraded25. Green star denotes the branch on which X–Y recombination was arrested and the Y chromosome diverged. None of the male morphs of P. parae are found in other species, making the most parsimonious explanation that all five morphs arose after recombination stopped. (Note, a version of the phylogeny in b is also presented in ref. 59).

Extended Data Fig. 2 Bayesian phylogeny built on presence/absence of the 27,950,090 P. parae Y-mers and the 646,754 P. picta Y-mers in each individual and rooted on P. picta (as in Fig. 2).

The posterior probability is presented at each node. The number of Y-mers each individual shares with P. picta Y-mers is denoted to the right. P. picta Y-mers are distributed across all morphs indicating that they have been segregating on non-recombining regions of the Y chromosome since recombination was stopped in the common ancestor of P. parae and P. picta.

Extended Data Fig. 3 Validation of morph-mer identification pipeline using random sets of individuals from each of the different morphs.

Different samples were used for each set except for blue where the 1 sample was used in validation set 2 and validation set 3. There were a low number of Y-mers unique to sets of four random individuals and zero Y-mers unique to sets with more than four individuals. This demonstrates the false positive rate of our morph-mer analysis was quite low because all major morphs had at least four individuals.

Extended Data Fig. 4 Mapping distribution for each set of morph-mers mapped to de novo scaffolds of males of that morph with no mismatches, gaps, or trimming.

There was a low incidence of individual morph-mers mapping to more than one scaffold (0 of the 59 Y-mers were contained in more than one scaffold across all males; 0 of the 1,435 parae-mers were contained in more than one scaffold in parae males; 131 of the 87,629 melanzona-mers were contained in more than one scaffold in melanzona males; 138 of the 64,515 immaculata-mers were contained in more than one scaffold in immaculata males). Left: cumulative morph-mers mapped for each individual, each change in hue is a different scaffold. A large percentage of morph-mers generally map to just one or a few scaffolds indicating that our k-mer approach reveals regions of highly diverged morph-specific sequence rather than single SNPs distributed throughout the genome. Right: cumulative morph-mers mapped presented as a function of the number of scaffolds. The strong deviation from 1:1 shows morph-mer mapping is non-random and further supports the morph-mers approach is identifying regions of morph-specific sequence. The total number of unique morph-mers identified for that morph is indicated in red on the axis (note the variation in number of morph-mers mapped is due to some individuals having morph-mers map to multiple scaffolds). Astrix in P02 of the melanzona-mers indicates the example alignment scaffold with melanzona-mers presented in Extended Data Fig. 5.

Extended Data Fig. 5 Melanzona-mers aligned to scaffold 104666 of sample P02 with no mismatches, gaps, or trimming.

Each 31 bp melanzona-mer is shown aligned below the reference sequence, and coverage is shown in purple above the reference sequence. Of the 87,629 unique melanzona-mers; 23,773 aligned to this scaffold. Regions of Ns are denoted on the reference genome in grey and explain a lack of melanzona-mers aligning to these regions. The strong clustering and overlapping nature of the melanzona-mers indicates sequence is highly diverged both from females and from the other morphs.

Extended Data Fig. 6 Morph-specific Y chromosome sequence is composed of significantly more interspersed repeats than the autosomes and X chromosome.

For males, only scaffolds containing >5 morph-specific Y-mers were evaluated, ensuring sequence is morph-specific and Y-linked. To determine rates of autosomes and X chromosomes, female full de novo genomes were evaluated. Stars indicate significant differences between morphs (* P<0.05, ** P<0.01).

Extended Data Fig. 7 Unrooted approximately-maximum-likelihood trees (FastTree) of each of the autosomes confirm that the extreme divergence across morphs is specific to the Y chromosome, and not the result of cryptic subpopulations.

Trees were built using the consensus sequence of the longest scaffold from each chromosome (as identified by RACA). Tips denote sample name, colour indicates morph, and numbers on branches indicate FastTree support value.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sandkam, B.A., Almeida, P., Darolti, I. et al. Extreme Y chromosome polymorphism corresponds to five male reproductive morphs of a freshwater fish. Nat Ecol Evol 5, 939–948 (2021). https://doi.org/10.1038/s41559-021-01452-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-021-01452-w

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing