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Multiple Origins of XY Female Mice (Genus Akodon): Phylogenetic And

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Multiple Origins of XY Female Mice (Genus Akodon): Phylogenetic And doi 10.1098/rspb.2000.1217 Multipleoriginsof XYfemalemice(genus Akodon): phylogeneticandchromosomalevidence HopiE. Hoekstra * and Scott V.Edwards Department of Zoology and Burke Museum, University of Washington, Seattle,WA98195,USA Despite the diversityin sex determination across organisms,theory predicts that the evolutionof XY females is rare inmammals dueto ¢ tness consequencesassociated with infertility orthe loss ofYY zygotes.W einvestigatedthis hypothesisfrom a phylogeneticperspective byexamining the inter- and intraspeci¢c distributionof Ychromosomes inmales andfemales (XY females) inSouth American ¢ eld mice (Akodon).Wefoundthat XYfemales occurredat appreciable frequencies (10^66%)in at least eight Akodon species, raisingthe possibilitythat this system ofsexdetermination has arisen multiple times inde- pendently.Todetermine the number oforigins of XY females in Akodon,weconstructed amolecular phylogenyof 1 6species of Akodon basedon mitochondrialDNA controlregion sequences. Bothparsimony andmaximum-likelihood reconstruction ofancestral states suggestthat multiple steps (gainsor losses of XYfemales) best explainthe evolutionof XY females, but donot clearly di¡ erentiate betweensingle and multiple origins.W ethen directlycompared functional and non-functional Y chromosomes insix species bySouthern blot analysis. W efoundthat maleand female Y chromosomerestriction fragmentlength poly- morphism patterns wereidentical within species, butalways di¡ ered betweenspecies, providingevidence that XYfemales aroseat least sixtimes withinthe Akodon lineage.T oourknowledge, this pattern in Akodon is the ¢rst documentationof a novelsex-determining system arisingmultiple times withina tight cladeof mammals. Inaddition, this system providesa cleartest ofthe accuracyof phylogenetic methods toreconstruct ancestralstates. Keywords: sexdetermination ;Ychromosome;sexchromosomes; XYfemales; ancestralstates; Akodon sex-determining mechanisms donot often evolve in species 1.INTRODUCTION withheteromorphic sex chromosomes likemammals Unlikemany basic developmental processes, the mechan- because(i) amale-determining mutation(formation of isms employedfor sex determination are highly diverse XXmales) faces the lackof necessary Y-chromosome across organisms(Ohno 1 967;Bull1985; Wibbels et al. genesfor male function, and (ii) afemale-determining 1994).Howsuch di¡erent sex-determining mechanisms mutation(formation of XY females) facesthe production aroseand diversi¢ ed has long puzzled biologists (Bull ofone-quarter YY o¡ spring and the potentialadverse 1985).Clearanswers to account for this diversityhave e¡ects ofY-chromosome genes on the feminizingprocess eludedscientists forthree primaryreasons: ¢ rst, the deep (Marin &Baker1 998).Thishypothesis predicts anevo- divergencebetween taxa with di¡ erent sex-determining lutionarilyconserved mechanism ofmammalian sex mechanisms complicatescomparative studies; second, determinationand very infrequent origins of novel sex- observinga sex-determining system earlyin its evolution determiningsystems, speci¢cally XX males orXY isdi¤cult; and¢ nally,the mechanisms ofsex determina- females. tionfor many clades are incompletely described, for SouthAmerican ¢ eldmice ( Akodon)present aunique examplereptiles, wherefewer than 10% of all species opportunityto study the evolutionof sex determination havebeen characterized (Viets et al.1994).Mammals becausethe aforementioneddi¤ culties areovercome by providean excellent system inwhich to study sex determi- the presence ofseveral closely related species inwhich nationbecause mechanisms areso well described across a XYfemales occur(see, forexample, Bianchi et al. 1971). varietyof species (Vorontsov et al.1980;F redga1 983). Inspecies withXY females, the presence orabsence of However,the diversityof sex determination is greatly the Ychromosomeno longer plays the decisiverole in sex reducedwithin mammals, whichgenerally employ a determination.In Akodon XYfemales, the Ychromosome system ofheterogametic (XY) males andhomogametic failsto trigger the malepathway and is hencereferred to (XX) females (Ohno1 967;Bull 1 983).Exceptionsto this as Y* (Lizarralde et al.1982).Evidencethat the causeof pattern generallyappear to have evolved once within a sex-reversal lies onthe Y * chromosomeincludes cytoge- genus.F orexample,the mole( Talpa; Sanchez et al. 1996), netic, molecular,breedingand phylogenetic studies, and whichhas hermaphroditic females; the woodlemming noindividuals of XYY * karyotypehave been reported (Myopus; Fredga et al.1976),whichhas XY females caused withinthis cladeof Akodon (Bianchi& Contreras1967; bya mutationon the Xchromosome;and¢ nally,asingle Lizarralde et al.1982;Vitullo et al.1986;Bianchi et al. species ofmicrotine vole( Microtus; Burgos et al. 1988), 1993;Espinosa & Vitullo1 996;H. E.Hoekstra,unpub- whichalso has XY females (fora review,see Fredga1 983). lisheddata) . Toexplainthe lackof diversity of sex-determining Inseveral species of Akodon, XY* females persist at schemes inmammals, Bull( 1983)suggested that novel highfrequency along with normal XX females innatural populations.Because XY * females occuronly in some *Author forcorrespondence ([email protected]) . species, the Akodon cladeallows us toaddress an Proc. R.Soc.Lond. B (2000) 267, 1825^1831 1825 © 2000The RoyalSociety Received 8 March 2000 Accepted 2 June 2000 1826H. E.Hoekstraand S. V.Edwards Multiple origins of XYfemale mice importantquestion regarding the evolutionof novel sex- primersequences are 1 2S1:5 ’-CGTTCATTGCTTAATTTTTAT determiningsystems that cannotbe addressed inother CACTGC-3’ and C2: 5’-TGGTCTTGTAAATCAGTAATG-3 ’. mammalianclades, namely ,howmany times didXY * PCR productswere cleaned using a puri¢cation kit ( Quiagen, females evolvein Akodon?Bull’s(1983)hypothesis predicts Valencia,CA, USA).Cyclesequencing using £ uorescently asingleancient origin of XY * females becausethe mode labelleddye terminators of both strands was carried out on an ofsex determination is aconservedtrait, whereasif sex ABI 373Aautomated sequencer. Sequences were aligned manu- determinationin Akodon ismore labile,XY * females may allyusing the program Sequencher ( GeneCodes)and adjusted haveevolved independently in several species. Inorder to byeye as necessary .Sequenceswere deposited in GenBank determine the number oforigins of the Y * chromosome, (accessionnumbers AF29 6258^AF296278). wetested aseries ofpredictions specifying single and Topologieswere generated using neighbour-joining (NJ) and multiple originsof the Y * chromosomeat both the species maximum-likelihood( ML)methods. T reeswere rooted by a andchromosomal levels (¢ gure 1 ).Weaddress these designatedoutgroup, Auliscomysp ictus ,anotherakodontine predictionsthrough a combinationof phylogeneticanalysis rodent(Smith & Patton1 993).Todevelopan empirical model of of Akodon species lineagesusing mitochondrial DN A sequenceevolution, ML constructionwas based on an initialNJ (mtDNA) controlregion sequences, aswell as an exami- treefrom which MLestimatesof ¬ (0.377;among-site rate nationof the ancestryof the Y * chromosomeitself. variation), µ (3.901;transitionbias) and the proportion of invar- iantsites (0.507) were generated. These values were then used in combinationwith anHKY85 model of sequence evolution, 2. METHODS which waschosen on the basis of hierarchical hypothesis testing (a) Tissue samples (Huelsenbeck& Rannala1997) ,togenerate an ML tree Samples of Akodonazarae and Akodonmolinae werecollected in (Voelker& Edwards1 998).Treetopologies and bootstrap Argentinaduring March ^April 1998.Remaining tissue samples supportwere generated using P AUP4.0(Swo¡ ord 1999) . fordetection of XY * femalesand phylogenetic reconstruction from1 4specieswere obtained from the Museum of V ertebrate (d) Reconstruction ofXY * evolution Zoology,Berkeley,CA; FieldMuseum of N aturalHistory , The presence(1 )orabsence (0) of XY * femaleswithin a Chicago,IL; National Museum of Natural History ,Washington, specieswas coded as a binarycharacter (Wiens 1 999)and DC;andMuseum of Southwestern Biology ,Albuquerque,NM. mappedon tothe ML topologyusing MacClade ( Maddison& Althoughthere are ca.25species of Akodon currentlydescribed Maddison1 992).Maximum-parsimony(MP) algorithmswere fromacross South America (Smith & Patton1 991),themajority usedto determine ancestral states. Ambiguous lineages were ofspecimens are inaccessible and not represented in museum resolvedusing the A CCTRAN (acceleratedtransitions) and collections.However, we havetissues from a geographically DELTRAN(delayed transitions) options of MacClade.ML esti- diversesample of well-described species from all of the major mationsof ancestral states were calculated using DISCRETE clades of Akodon (seeAppendix A) . 1.01b(Pagel1994, 1997) .Ratesof characterchange and ML esti- matesof ancestral character states were calculated following (b) Screening for XY * females Mooers& Schulters(1 999)using branch lengths estimated from Todetectthe presence of XY * females in Akodon species,poly- theNJ tree. Because DISCRETE does not handle unknown merasechain reaction ( PCR)genotyping was performed on 1 79 states,the unknown tips were either assigned state by MP ,or phenotypicfemales from 16 species of Akodon.PCR primers alternativelyall possible permutations were averaged. designedto amplify an intronof the Smcy geneon the Y chromo- someof mammals (Agulnik et al.1994)were used to determine (f) Southern blotanalysis thepresence or absence of theY * chromosomein phenotypically Highmolecular weight DNA was isolated
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