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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

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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.

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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.

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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

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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.

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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

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  1. Benjamin A. Sandkam
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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.

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Correspondence to Benjamin A. Sandkam.

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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.

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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

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