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Extreme Heterogeneity in Sex Chromosome bioRxiv preprint doi: https://doi.org/10.1101/589788; this version posted March 28, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 1 Extreme'heterogeneity'in'sex'chromosome'differentiation'and'dosage' 2 compensation'in'livebearers' 3 ' 4 Iulia!Darolti1,!Alison!E.!Wright2,!Benjamin!A.!Sandkam3,!Jake!Morris1,!Natasha!I.!Bloch4,! 5 Marta!Farré5,!Rebecca!C.!Fuller6,!Godfrey!R.!Bourne7,!Denis!M.!Larkin8,!Felix!Breden9,!Judith! 6 E.!Mank1,3,10! 7 ! 8 ! 9 1!Department!of!Genetics,!Evolution!and!Environment,!University!College!London,!UK! 10 2!Department!of!Animal!and!Plant!Sciences,!University!of!Sheffield,!UK! 11 3!Department!of!Zoology,!University!of!British!Columbia,!Canada! 12 4!Department!of!Biomedical!Engineering,!University!of!Los!Andes,!Colombia!! 13 5!School!of!Biosciences,!University!of!Kent,!UK! 14 6!Department!of!Animal!Biology,!University!of!Illinois!at!UrbanaYCampaign,!USA! 15 7!Department!of!Biology,!University!of!Missouri!St.!Louis,!USA! 16 8!Comparative!Biomedical!Sciences!Department,!Royal!Veterinary!College,!UK!! 17 9!Department!of!Biological!Science,!Simon!Fraser!University,!Canada! 18 10!Department!of!Organismal!Biology,!Uppsala!University,!Sweden! 19 ! 20 ! 21 Corresponding!author:!Iulia!Darolti,!eYmail:[email protected] ! 1! bioRxiv preprint doi: https://doi.org/10.1101/589788; this version posted March 28, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 22 ABSTRACT' 23 Once!recombination!is!halted!between!the!X!and!Y!chromosome,!sex!chromosomes!begin!to! 24 differentiate!and!transition!to!heteromorphism.!While!there!is!a!remarkable!variation!across! 25 clades!in!the!degree!of!sex!chromosome!divergence,!far!less!is!known!about!variation!in!sex! 26 chromosome!differentiation!within!clades.!Here,!we!combined!whole!genome!and! 27 transcriptome!sequencing!data!to!characterise!the!structure!and!conservation!of!sex! 28 chromosome!systems!across!Poeciliidae,!the!livebearing!clade!that!includes!guppies.!We! 29 found!that!the!Poecilia(reticulata!XY!system!is!much!older!than!previously!thought,!being! 30 shared!not!only!with!its!sister!species,!Poecilia(wingei,!but!also!with!Poecilia(picta,!which! 31 diverged!30!mya.!Despite!the!shared!ancestry,!we!uncovered!an!extreme!heterogeneity! 32 across!these!species!in!the!proportion!of!the!sex!chromosome!with!suppressed! 33 recombination,!and!the!degree!of!Y!chromosome!decay.!The!sex!chromosomes!in!P.( 34 reticulata!are!largely!homomorphic,!with!recombination!persisting!over!a!substantial! 35 fraction.!However,!the!sex!chromosomes!in!P.(picta!are!completely!nonYrecombining!and! 36 strikingly!heteromorphic.!In!addition!to!being!highly!divergent,!the!sex!chromosome!system! 37 in!P.(picta!includes!a!neoYsex!chromosome,!the!result!of!a!fusion!between!the!ancestral!sex! 38 chromosome!and!part!of!chromosome!7.!Remarkably,!the!profound!degradation!of!the! 39 ancestral!Y!chromosome!in!P.(picta!is!counterbalanced!by!the!evolution!of!complete!dosage! 40 compensation!in!this!species,!the!first!such!documented!case!in!teleost!fish.!Our!results! 41 offer!important!insight!into!the!initial!stages!of!sex!chromosome!evolution!and!dosage! 42 compensation.! ! ! 2! bioRxiv preprint doi: https://doi.org/10.1101/589788; this version posted March 28, 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 4.0 International license. 43 INTRODUCTION' 44 Sex!chromosome!evolution!is!characterized!by!remarkable!variation!across!lineages!in!the! 45 degree!of!divergence!between!the!X!and!Y!chromosomes!(1,!2).!Derived!from!a!pair!of! 46 homologous!autosomes,!sex!chromosomes!begin!to!differentiate!as!recombination!between! 47 them!is!supressed!in!the!heterogametic!sex!over!the!region!spanning!a!newly!acquired!sexY 48 determining!locus!(3,!4).!The!lack!of!recombination!exposes!the!sexYlimited!Y!chromosome! 49 to!a!range!of!degenerative!processes!that!cause!it!to!diverge!in!structure!and!function!from! 50 the!corresponding!X!chromosome,!which!still!recombines!in!females!(5,!6).!Consequently,! 51 the!sex!chromosomes!are!expected!to!eventually!transition!from!a!homomorphic!to!a! 52 heteromorphic!structure,!supported!by!evidence!from!many!of!the!old!and!highly! 53 differentiated!systems!found!in!mammals!(7,!8),!birds!(9),!Drosophila!(5)!and!snakes!(10).!! 54 However,!there!is!a!significant!heterogeneity!among!clades,!and!even!among!species!with! 55 shared!sex!chromosome!systems,!in!the!spread!of!the!nonYrecombining!region,!and!the! 56 subsequent!degree!of!sex!chromosome!divergence!(11,!12).!Age!does!not!always!reliably! 57 correlate!with!the!extent!of!recombination!suppression,!as!in!some!species!the!sex! 58 chromosomes!maintain!a!largely!homomorphic!structure!over!long!evolutionary!periods! 59 (12Y16),!while!in!others!the!two!sex!chromosomes!are!relatively!young,!yet!profoundly! 60 distinct!(17).!Comparing!the!structure!and!recombination!patterns!of!sex!chromosomes! 61 between!closely!related!species!is!a!powerful!method!to!determine!the!forces!shaping!sex! 62 chromosome!evolution!over!time.! 63 Sex!chromosome!divergence!can!also!lead!to!differences!in!X!chromosome!gene!dose! 64 between!males!and!females.!Following!recombination!suppression,!the!Y!chromosome! 65 undergoes!gradual!degradation!of!gene!activity!and!content,!leading!to!reduced!gene!dose! 66 in!males!(6,!18,!19).!Genetic!pathways!that!incorporate!both!autosomal!and!sexYlinked! 67 genes!are!primarily!affected!by!such!imbalances!in!gene!dose,!with!potential!severe! 68 phenotypic!consequences!for!the!heterogametic!sex!(20).!In!some!species,!this!process!has! 69 led!to!the!evolution!of!chromosomeYlevel!mechanisms!to!compensate!for!the!difference!in! 70 gene!dose!(21,!22).!However,!the!majority!of!sex!chromosome!systems!are!associated!with! 71 geneYbyYgene!level!mechanisms,!whereby!dosage!sensitive!genes!are!compensated,!but! 72 overall!expression!of!the!X!chromosome!is!lower!in!males!compared!to!females!(19,!22,!23).!! ! 3! bioRxiv preprint doi: https://doi.org/10.1101/589788; this version posted March 28, 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 4.0 International license. 73 As!opposed!to!most!mammals!and!birds,!the!sex!chromosomes!in!many!fish,!lizard!and! 74 amphibian!species!are!characterized!by!a!lack!of!heteromorphism,!which!has!been! 75 attributed!to!processes!such!as!sex!chromosome!turnover!and!sex!reversal!(15,!24Y28).!As!a! 76 result,!closely!related!species!from!these!taxonomic!groups!often!have!a!variety!of!sex! 77 chromosome!systems!found!at!different!stages!in!evolution!(26,!29).!Additionally,!global! 78 dosage!compensation!has!not!yet!been!found!in!fish,!perhaps!due!to!the!transient!nature!of! 79 the!sex!chromosome!systems!and!the!general!lack!of!heteromorphism!in!the!group.! 80 However,!incomplete!dosage!compensation,!through!a!geneYbyYgene!regulation! 81 mechanism,!may!have!evolved!in!sticklebacks!(30)!and!flatfish!(31).!! 82 Poeciliid!species!have!been!the!focus!of!many!studies!concerning!sex!determination!(25).! 83 Moreover,!many!poeciliids!exhibit!sexual!dimorphism,!with!some!colour!patterns!and!fin! 84 shapes!controlled!by!sexYlinked!loci!(32Y36).!The!clade!also!has!a!diversity!of!genetic!sex! 85 determination!systems,!with!both!male!and!female!heterogametic!sex!chromosomes! 86 observed!in!different!species!(37,!38).!Most!work!on!Poeciliid!sex!chromosome!structure!has! 87 focused!on!the!Poecilia(reticulata!XY!system,!positioned!on!chromosome!12!(39)!which! 88 shows!very!low!levels!of!divergence!(35,!40).!Although!recombination!is!suppressed!over! 89 almost!half!the!length!of!the!P.(reticulata!sex!chromosome,!there!is!little!sequence! 90 differentiation!between!the!X!and!Y!chromosomes!and!no!perceptible!loss!of!gene!activity! 91 of!YYlinked!genes!in!males!(40).!This!low!level!of!divergence!suggests!a!recent!origin!of!the! 92 sex!chromosome!system.!! 93 There!is!intraYspecific!variation!in!the!extent!of!the!nonYrecombining!region!within(P.( 94 reticulata,!correlated!with!the!strength!of!sexual!conflict!(40).!Additionally,!although!P.( 95 reticulata!and!its!sister!species,!P.(wingei,!are!thought!to!share!an!ancestral!sex! 96 chromosome!system!(41,!42),!there!is!some!evidence!for!variation!in!Y!chromosome! 97 divergence!between!these!species!(42).!It!is!unclear!whether!the!XY!chromosomes!maintain! 98 the!same!level!of!heteromorphism!in!other!poeciliids!(37,!41),!or!even!whether!they!are! 99 homologous,!to!the!sex!chromosomes!in!P.(reticulata.!! 100 Here!we!perform!comparative!genome!and!transcriptome!analyses!on!multiple!Poeciliid! 101 species!to!test!for!conservation!and!turnover!of!sex!chromosome!systems!and!investigate! 102 patterns!of!sex!chromosome!differentiation!in!the!clade.!We!find!the!XY!system!in!P.( ! 4! bioRxiv preprint doi: https://doi.org/10.1101/589788; this version posted March 28, 2019. 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