The balanced lethal system of crested newts: A ghost of sex chromosomes past?

Balanced lethal systems are more than biological curiosities: as theory predicts, they should quickly be eliminated through the joint forces of recombination and selection. That such systems might become fixed in natural populations poses a challenge to evolutionary theory. Here we address the case of a balanced lethal system fixed in crested newts and related species, which makes 50% of offspring die early in development. All adults are heteromorphic for chromosome pair 1. The two homologues (1A and 1B) have different recessive deleterious alleles fixed on a nonrecombining segment, so that heterozygotes are viable, while homozygotes are lethal. Given such a strong segregation load, how could autosomes stop recombining? We propose a role for a sex-chromosome turnover from pair 1 (putative ancestral sex chromosome) to pair 4 (currently active sex chromosome). Accordingly, 1A and 1B represent two variants (Y(A) and Y(B)) of the Y chromosome from an ancestral male-heterogametic system. We formalize a scenario in which turnovers are driven by sex ratio selection stemming from gene-environment interactions on sex determination. Individual-based simulations show that a balanced lethal system can be fixed with significant likelihood, provided the masculinizing allele on chromosome 4 appears after the elimination of the feminizing allele on chromosome 1. Our study illustrates how strikingly maladaptive traits might evolve through natural selection. DOI: https://doi.org/10.1086/668076 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-73280 Published Version Originally published at: Grossen, Christine; Neuenschwander, Samuel; Perrin, Nicolas (2012). The balanced lethal system of crested newts: A ghost of sex chromosomes past? The American Naturalist, 180(6):E174-E183. DOI: https://doi.org/10.1086/668076 ! "# $ %&'$ ()*+, '$ ".$'/ 01 )'$)*% 2+ ,)()')( '3 '$4 + ,5'$5 1,)'' 69% (: : '! . " ,6 "-5!) '3 ,,5 7 <=>?@ABCD?ECFGHIFJFKLAEMHNFJOCPFEQREPN?BSPCLFGTAOSAEE?QUV<W<XTAOSAEE?QYZPC[?BJAEM\]=̂ESCPCOC?FGHNFJOCPFEABL_PFJFKL AEMHENPBFED?ECAJYCOMP?SQREPN?BSPCLFG̀OaBPIbQUVcWXd̀ OaBPIbQYZPC[?BJAEM\e=fPCAJĝhQYZPSŜESCPCOC?FG_PFPEGFBDACPISQREPN?BSPCL FGTAOSAEE?QUV<W<XTAOSAEE?QYZPC[?BJAEM ijklmnopqokrjsrtuvwxyuxz{||o}nop{j~jn€wxyuxz‚o|nrƒ„m|s‚t}jk‚m…op†|nƒkorx‡wxyux ˆrtsppsns‰bC@Š‹MŒ=MFP=FBK‹<W=XW<‹MBLAM=eEŽdd= Š_AJAEI?MJ?CbAJSLSC?DSAB?DFB?CbAEPFJFKPIAJIOBPg FSPCP?SŠASCb?FBL@B?MPICSQCb?LSbFOJMOPI‘JL??JPDPEAC?MCbBFOKb Cb?’FPECGFBI?SFGB?IFDPEACPFEAEMS?J?ICPFE=hbACSOIbSLSC?DS DPKbC?IFD?“Œ?MPEEACOBAJ@F@OJACPFES@FS?SAIbAJ?EK?CF?NFg JOCPFEABLCb?FBL=V?B?Z?AMMB?SSCb?IAS?FGAAJAEI?MJ?CbAJSLSC?D “Œ?MPEIB?SC?ME?ZCSAEMB?JAC?MS@?IP?SQZbPIbDA‘?SXW” FG FGS@BPEKMP??ABJLPEM?N?JF@D?EC=•JAMOJCSAB?b?C?BFDFB@bPIGFB IbBFDFSFD?@APB<=hb?CZFbFDFJFKO?S–<•AEM<_—bAN?MPG?B?EC B?I?SSPN?M?J?C?BPFOSAJ?J?S“Œ?MFEAEFEB?IFDPEPEKS?KD?ECQSF CbACb?C?BF[LKFC?SAB?NPAJ?QZbPJ?bFDF[LKFC?SAB?J?CbAJ=˜PN?E SOIbASCBFEKS?KB?KACPFEJFAMQbFZIFOJMAOCFSFD?SSCF@B?IFDg PEPEK™š?@BF@FS?ABFJ?GFBAS?ŒgIbBFDFSFD?COBEFN?BGBFD@APB <–@OCACPN?AEI?SCBAJS?ŒIbBFDFSFD?—CF@APB›–IOBB?ECJLAICPN?S?Œ IbBFDFSFD?—=•IIFBMPEKJLQ<•AEM<_B?@B?S?ECCZFNABPAECS–œ• AEMœ_—FGCb?œIbBFDFSFD?GBFDAEAEI?SCBAJDAJ?gb?C?BFKAD?CPI SLSC?D=š?GFBDAJP[?ASI?EABPFPEZbPIbCOBEFN?BSAB?MBPN?EL S?ŒBACPFS?J?ICPFESC?DDPEKGBFDK?E?g?ENPBFED?ECPEC?BAICPFESFE S?ŒM?C?BDPEACPFE=̂EMPNPMOAJgAS?MSPDOJACPFESSbFZCbACAAJg AEI?MJ?CbAJSLSC?DIAE?“Œ?MZPCbSPKEP“IAECJP‘?JPbFFMQ@BFNPM?M Cb?DASIOJPEP[PEKAJ?J?FEIbBFDFSFD?›A@@?ABSAGC?BCb??JPDPg EACPFEFGCb?G?DPEP[PEKAJ?J?FEIbBFDFSFD?<=OBSCOMLPJOSg CBAC?SbFZSCBP‘PEKJLDAJAMA@CPN?CBAPCSDPKbC?NFJN?CbBFOKbEACOBAJ S?J?ICPFE= žotŸƒrp‰AJAEI?MJ?CbAJSLSC?DQDAJAMA@CPN?CBAPCQS?ŒIbBFDFSFD? COBEFN?BSQS?ŒBACPFS?J?ICPFE=