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A Bird's White-Eye View on Avian Sex Chromosome Evolution

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A Bird's White-Eye View on Avian Sex Chromosome Evolution bioRxiv preprint doi: https://doi.org/10.1101/505610; this version posted January 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 A BIRD'S WHITE-EYE VIEW ON AVIAN SEX 2 CHROMOSOME EVOLUTION 3 4 Thibault Leroy1, Yoann Anselmetti1, Marie-Ka Tilak1, Sèverine Bérard1, Laura Csukonyi1,2, Maëva 5 Gabrielli2, Céline Scornavacca1, Borja Milá3, Christophe Thébaud2, Benoit Nabholz1* 6 7 1 ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France 8 2 Laboratoire Evolution et Diversité Biologique (EDB), UMR 5174 CNRS – Université Paul Sabatier – IRD, Toulouse, 9 France 10 3 National Museum of Natural Sciences (MNCN), Spanish National Research Council (CSIC), Madrid, Spain 11 * Corresponding author: [email protected] 12 13 14 41 diversity in both translocated regions and, as expected, 15 ABSTRACT 42 even more so on the neoW chromosome. In order to 16 43 compare the rates of molecular evolution in genomic 44 regions of the autosomal-to-sex transitions, we then 17 Chromosomal organization is relatively stable 45 estimated the ratios of non-synonymous to 18 among avian species, especially with regards to sex 46 synonymous polymorphisms (πN/πS) and substitutions 19 chromosomes. Members of the large Sylvioidea clade 47 (dN/dS). Based on both ratios, no or little contrast 20 however have a pair of neo-sex chromosomes which is 48 between autosomal and Z genes was observed, thus 21 unique to this clade and originate from a parallel 49 representing a very different outcome than the higher 22 translocation of a region of the ancestral 4A 50 ratios observed at the neoW genes. In addition, we 23 chromosome on both W and Z chromosomes. Here, 51 report significant changes in base composition content 24 we took advantage of this unusual event to study the 52 for translocated regions on the W and Z chromosomes 25 early stages of sex chromosome evolution. To do so, 53 and a large accumulation of transposable elements 26 we sequenced a female (ZW) of two Sylvioidea species, 54 (TE) on the newly W region. Our results revealed 27 a Zosterops borbonicus and a Z. pallidus. Then, we 55 contrasted signals of molecular evolution changes 28 organized the Z. borbonicus scaffolds along 56 associated to these autosome-to-sex transitions, with 29 chromosomes and annotated genes. Molecular 57 congruent signals of a W chromosome degeneration 30 phylogenetic dating under various methods and 58 yet a surprisingly weak support for a fast-Z effect. 31 calibration sets confidently confirmed the recent 32 diversification of the genus Zosterops (1-3.5 million 59 33 years ago), thus representing one of the most 34 exceptional rates of diversification among vertebrates. 60 35 We then combined genomic coverage comparisons of 61 Key-words : Sex chromosome, molecular evolution, 36 five males and seven females, and homology with the 62 molecular dating, bird diversification, Sylvioidae, 37 zebra finch genome (Taeniopygia guttata) to identify 63 Zosterops. 38 sex chromosome scaffolds, as well as the candidate 39 chromosome breakpoints for the two translocation 40 events. We observed reduced levels of within-species bioRxiv preprint doi: https://doi.org/10.1101/505610; this version posted January 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 42 chromosomes (so-called fast-X or fast-Y effects) (Mank et 1 INTRODUCTION 43 al. 2007; Rousselle et al. 2016). In addition, given that 44 mutations are on average recessive, positive selection is 45 expected to be more efficient in the heterogametic sex 2 Spontaneous autosomal rearrangements are 46 (Hvilsom et al. 2012; Nam et al. 2015). Suppression of 3 common across higher metazoan lineages (Choghlan et 47 recombination is also expected to initiate a degenerative 4 al. 2005). By contrast, sex chromosome architectures are 48 process on the Y chromosome, that may result in the 5 much more conserved, even across distant lineages 49 accumulation of nonsynonymous deleterious 6 (Murphy et al. 1999; Raudsepp et al. 2004; Fraïsse et al. 50 substitutions owing to a series of processes acting 7 2017). A growing number of studies have recently 51 simultaneously: Muller’s ratchet, the Hill-Robertson 8 observed departures from this pattern of evolutionary 52 effect, and positive and background selection 9 conservation by detecting changes in the genomic 53 (Charlesworth and Charlesworth, 2000). For the same 10 architecture of sex chromosomes in some particular 54 reason, transposable elements (TEs) are also expected to 11 lineages - so-called neo-sex chromosomes that are – 55 accumulate soon after the cessation of recombination in 12 mainly generated by fusion or translocation events of at 56 the Y chromosomes (Charlesworth 1991; Charlesworth et 13 least one sex chromosome with an autosome (e.g. Kitano 57 al. 1994). 14 & Peichel, 2012; Zhou & Bachtrog, 2012). Considering the 15 long-term conservation of sex chromosome synteny, 58 Except for few reported examples (de Oliveira et 16 neo-sex chromosomes provide opportunities to 59 al. 2005; Nanda et al. 2006; Kapusta & Suh, 2017; 17 investigate the processes at work during the early stages 60 O’Connor et al. 2018), all birds share a high degree of 18 of sex chromosome evolution (Charlesworth et al. 2005). 61 synteny conservation across autosomal chromosomes 19 Previous detailed studies have for example investigated 62 (Griffin et al. 2007; Nanda et al. 2008; Ellegren, 2010; 20 its important role for divergence and speciation (e.g. 63 Völker et al. 2010; Warren et al. 2010; Ellegren, 2013) 21 Kitano et al. 2009; Yoshida et al. 2014; Bracewell et al. 64 and even more at the Z chromosome (Nanda et al. 2008). 22 2017). 65 A notable exception is the neo-sex chromosome of 66 Sylvioidea species, a superfamily of passerine birds in 23 From a molecular evolution point of view, an 67 which a translocation of a large part of the Zebra finch 4A 24 important consequence of the transition from autosomal 68 chromosome onto both the W and the Z chromosomes, 25 to sex chromosome is the reduction in effective 69 as characterized by genetic mapping (hereafter 26 population size (N ). Assuming a 1:1 sex ratio, N of e e 70 translocations of the neoW-4A and neoZ-4A on ancestral 27 transposed regions on the Y (or W) and X (or Z) 71 neoW-W and neoZ-Z respectively; Pala et al. 2012a). 28 chromosomes are expected to decrease by three-fourths 72 These two autosome-to-sex chromosome transitions are 29 and one-fourths, respectively (see Ellegren, 2009 for 73 present in reed warblers (Acrocephalidae), old-world 30 details). According to the neutral theory, nucleotide 74 warblers (Sylviidae) and larks (Alaudidae) (see also 31 diversity is then expected to be reduced proportionally 75 Brooke et al. 2010), and therefore likely occurred in the 32 to the reduction in N due to increased drift effects e 76 common ancestor of all present-day Sylvioidea (Pala et 33 (Vicoso & Charlesworth, 2006; Pool & Nielsen, 2007). N e 77 al. 2012a,b; Sigeman et al. 2018), between 15 and 30 34 reduction also induces a change in the balance between 78 million years ago (Myrs) (Ericson et al. 2014; Prum et al. 35 selection and drift, with drift playing a greater role after 79 2015; Nabholz et al. 2016). These two sex chromosome 36 the translocation, thus reducing the efficacy of natural 80 translocations provide unique opportunities to 37 selection to purge deleterious mutations from 81 investigate the early stages of the W and Z chromosome 38 populations. Mutations - including deleterious ones - 82 evolution. 39 may also drift to fixation at a faster rate in sex- 83 Based on phylogenetic trees calibrated using 40 chromosomes than in autosomes, thus generating 84 geological events (Moyle et al. 2009), Zosterops species 41 expectations for faster evolution at X and Y 85 of the family Zosteropidae (more commonly referred to bioRxiv preprint doi: https://doi.org/10.1101/505610; this version posted January 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 86 as white-eyes) are considered to have emerged around 130 for a substantial loss of diversity on both translocated 87 the Miocene/Pliocene boundary. Considering both this 131 regions, largely consistent with expectations under 88 recent emergence and the remarkable high diversity 132 neutral theory. We then compared patterns of 89 currently observed in this genus (more than 80 species), 133 polymorphisms and divergence at neo-sex 90 this group appears to have one of the highest 134 chromosome genes and found support for a 91 diversification rates reported to date for vertebrates and 135 considerable fast-W effect, but surprising weak support 92 is therefore considered as one of the ‘great speciator’ 136 for a fast-Z effect. Investigations of candidate changes 93 examples (Diamond et al. 1976; Moyle et al. 2009). 137 in base led to the identification of specific signatures 94 White-eye species are typical examples of taxa spanning 138 associated with abrupt changes in recombination rates 95 the entire “grey zone” of speciation (Roux et al. 2016). As 139 (reduction or cessation) of the two neo-sex regions.
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