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Divergence and Remarkable Diversity of the Y Chromosome in Guppies

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Divergence and Remarkable Diversity of the Y Chromosome in Guppies bioRxiv preprint doi: https://doi.org/10.1101/2020.07.13.200196; this version posted July 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Divergence and Remarkable Diversity of the Y Chromosome in 2 Guppies 3 Pedro Almeida1, Benjamin A. Sandkam2, Jake Morris1, Iulia Darolti2, Felix Breden3, 4 Judith E. Mank1,2 5 1. Department of Genetics, Evolution and Environment, University College London, 6 London, U.K. 7 2. Department of Zoology and Biodiversity Research Centre, University of British 8 Columbia, Vancouver, Canada 9 3. Department of Biological Sciences, Simon Fraser University, Burnaby, Canada 10 11 12 13 14 15 Keywords: 16 Poecilia reticulata, sex chromosomes, Y haplotypes, recombination suppression, linked- 17 reads 18 19 20 21 22 23 24 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.13.200196; this version posted July 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 25 Abstract 26 The guppy sex chromosomes show an extraordinary diversity in divergence across 27 populations and closely related species. In order to understand the dynamics of the 28 guppy Y chromosome, we used linked-read sequencing to assess Y chromosome 29 evolution and diversity across upstream and downstream population pairs that vary in 30 predator and food abundance in three replicate watersheds. Based on our population- 31 specific genome assemblies, we first confirmed and extended earlier reports of two 32 strata on the guppy sex chromosomes. Stratum I shows significant accumulation of 33 male-specific sequence, consistent with Y divergence, and predates the colonization of 34 Trinidad. In contrast, Stratum II shows divergence from the X, but no Y-specific 35 sequence, and this divergence is greater in three replicate upstream populations 36 compared to their downstream pair. Despite longstanding assumptions that sex 37 chromosome recombination suppression is achieved through inversions, we find no 38 evidence of inversions associated with either Stratum I or Stratum II. Instead, we 39 observe a remarkable diversity in Y chromosome haplotypes within each population, 40 even in the ancestral Stratum I. This diversity is likely due to gradual mechanisms of 41 recombination suppression, which, unlike an inversion, allow for the maintenance of 42 multiple haplotypes. In addition, we show that this Y diversity is dominated by low- 43 frequency haplotypes segregating in the population, suggesting a link between 44 haplotype diversity and female-preference for rare Y-linked colour variation. Our results 45 reveal the complex interplay between recombination suppression and Y chromosome 46 divergence at the earliest stages of sex chromosome divergence. 47 48 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.13.200196; this version posted July 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 49 Introduction 50 Sex chromosomes diverge from each other once recombination between the X and Y 51 chromosome is halted 1,2. Despite the prevalence and repeated origin of sex 52 chromosomes 3, we still know little about the initial stages of X-Y divergence. In 53 particular, it remains unclear exactly how recombination is suppressed between 54 emerging sex chromosomes. Classic models assume that recombination is instantly 55 and completely arrested when one chromosome undergoes an inversion 4. However, 56 empirical studies have suggested that the earliest stages of recombination suppression 57 may be due to shifts in local recombination hotspots 5, which could, at least initially, 58 provide an incomplete barrier to recombination. Moreover, inversions are rare events, 59 and fixation of a Y-linked inversion as a mechanism to achieve recombination 60 suppression would lead to a limited number of Y haplotypes. If recombination is 61 curtailed through means other than an inversion, substantial initial haplotype diversity 62 can persist within the non-recombining region. The mechanism of recombination 63 suppression can leave fundamentally different patterns of diversity on emerging Y 64 chromosomes. 65 Observations of Y-linked male colour traits in guppies (Poecilia reticulata) 6–10, helped 66 inspire theories of sex chromosome formation 11, and observations that Y-linkage of 67 colour varies by population 6,12–14 have fuelled speculation of a link between sex 68 chromosome divergence and female preference for Y-linked male colour combinations 69 15–18. Curiously, there appears to be a surprising diversity of Y-linked colour haplotypes 70 19,20 which is somewhat counterintuitive as the combination of purifying selection and 71 linkage effects on Y chromosomes typically combine to remove diversity from these 72 regions 21. 73 Guppies have recently resurfaced as a model for the genomic study of sex chromosome 74 formation. Recent work has suggested that P. reticulata shows evidence of early Y 75 degeneration at the distal end of Chromosome 12, in a region that is also ancestral to 76 Poecilia wingei, its sister species (Stratum I) 15,17,22–24. This non-recombining region is 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.13.200196; this version posted July 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 77 consistent with previous cytogenetic and linkage studies 8,9,25–28, and a genetic map of 78 the sex determining region 29. In addition, the extent of X-Y divergence varies 79 substantially among populations of P. reticulata and between P. reticulata and P. wingei 80 15,22,24. This suggests that recombination is also rare beyond Stratum I, either because 81 recombinants are selected against in natural populations, or the rate of recombination is 82 sufficiently low that does not fully counter the accumulation of Y-specific mutations. 83 However, it is important to note that others have not recovered support for this region of 84 recombination suppression using slightly different genomic approaches 16, and it has 85 been suggested that the guppy Y chromosome lacks any discernible divergence from 86 the X, despite cytogenetic work showing X-Y differentiation 30–32. 87 The guppy sex chromosome system is surprisingly old, as it is shared with Poecilia picta 88 22, suggesting it originated at least 20 million years ago 33. The age of the sex 89 chromosome system, coupled with the fact that the sex chromosomes in P. picta are 90 highly diverged and possess a mechanism of complete X chromosome dosage 91 compensation in males 22, indicates that other forces are counteracting the 92 degeneration normally associated with non-recombining regions to maintain the overall 93 integrity of the Y in P. reticulata. 94 In the northern range mountains of Trinidad, downstream and upstream river 95 populations are known to differ in male colour patterns and other important life-history 96 traits due to differences in predator and food abundance 34,35, and these complex 97 phenotypes have been shown to evolve rapidly and repeatedly 36. In order to 98 understand sex chromosome divergence in this system, identify Y-specific sequence, 99 and determine the mechanism of recombination suppression, we generated linked-read 100 sequences from multiple males and females from both upstream and downstream 101 population pairs from three rivers in Trinidad, and used these data to build high-quality 102 population-specific genome assemblies. 103 Given the controversy over the extent of X-Y divergence in this species 15–18, we first 104 independently replicated our previous results 15,22. We again recovered evidence of both 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.13.200196; this version posted July 13, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 105 a region of X-Y divergence shared among populations (Stratum I), and a convergently 106 evolved region of greater X-Y divergence in upstream compared to downstream 107 populations (Stratum II). We then use linked-read assemblies to show a significant 108 accumulation of male-specific sequence and male-linked SNPs in Stratum I, and reveal 109 an astonishing diversity in Y haplotype sequence both among and within populations. 110 We show that this diversity is not associated with an inversion, and instead suggest that 111 the lack of a structural mechanism of recombination suppression allows for the 112 maintenance of large numbers of Y haplotypes. Taken together, our results reveal the 113 initial stages of sex chromosome divergence and the evolutionary processes that allow 114 Y diversity to be maintained. 115 116 Results 117 We collected and obtained whole-genome sequencing reads for 120 wild-caught 118 individuals, 20 male and 20 female P. reticulata samples for each of the Aripo, Quare 119 and Yarra rivers in Trinidad, equally divided between downstream and upstream 120 populations. We used a combination of 10x Genomics linked-read sequencing and 121 paired-end Illumina sequencing (see Materials and Methods and Supplementary Table 122 S1), and after filtering alignments to the reference genome (see Materials & Methods), 123 we recovered an average effective coverage of ~30X for each male and ~20X for each 124 female. 125 In order to remove potentially confounding effects of the underlying genetic variation 126 between rivers, we constructed river-specific reference genomes using the best female 127 linked-reads’ de-novo assembly, based on scaffold N50 and phase block N50 values 128 (Supplementary Table S2). In all cases, these assemblies showed a high completeness 129 and contiguity with N50 of >1 Mb, 3 Mb and 8 Mb for Yarra, Aripo and Quare genomes, 130 respectively 37 (Supplementary Table S3).
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