Article A Haploid System of Sex Determination in the Brown Alga Ectocarpus sp.

Genomics Research Institute, University of Pretoria,Hatfield Campus, Pretoria 0028, South AfricaSummaryBackground: Acommon feature of mostgenetic sex-determi-nationsystemsstudiedsofaristhatsexisdeterminedbynon-recombining genomic regions, which can be of various sizesdepending on the species. These regions have evolved inde-pendently and repeatedly across diverse groups. A numberof such sex-determining regions (SDRs) have been studied inanimals, plants, and fungi, but very little is known about theevolution of sexes in other eukaryotic lineages.Results:Wereportherethesequencing andgenomicanalysisoftheSDRofEctocarpus,abrownalgathathasbeenevolvingindependently from plants, animals, and fungi for over onegiga-annum. In Ectocarpus, sex is expressed during thehaploid phase of the life cycle, and both the female (U) andthe male (V) sex chromosomes contain nonrecombining re-gions. The U and V of this species have been diverging formore than 70 mega-annum, yet gene degeneration has beenmodest, and the SDR is relatively small, with no evidence forevolutionary strata. These features may be explained by theoccurrence of strong purifying selection during the haploidphase of the life cycle and the low level of sexual dimorphism.V is dominant over U, suggesting that femaleness may be thedefault state, adopted when the male haplotype is absent.Conclusions: The Ectocarpus UV system has clearly had adistinct evolutionary trajectory not only to the well-studiedXY and ZW systems but also to the UV systems describedso far. Nonetheless, some striking similarities exist, indicatingremarkable universality of the underlying processes shapingsex chromosome evolution across distant lineages.IntroductionGenetic determination of sex is mediated by sex-determiningregions (SDRs) of various sizes or by sex chromosomes in abroad range of eukaryotes. Sex chromosomes have arisenindependently and repeatedly across the eukaryotic tree,and comparative analysis of different sex-determination sys-tems has provided insights into how these systems originateand evolve. A typical sex chromosome pair is thought tohave derivedfrom apair of autosomes through theacquisitionof genes involved in sex determination. If more than one locusinvolved in sex determination is located on the chromosome,recombination between loci is expected to be suppressedto avoid the production of maladapted individuals with acombinationof male andfemale alleles ofthe sex-determininggenes. This leads to the establishment of a nonrecombiningregion on the nascent sex chromosome, with important con-sequences for the evolution of this region of the genome [1].For example, as a result of the suppression of recombinationwithin the SDR, repetitive DNA tends to accumulate, leadingto an increase in SDR size and degeneration of genes withinthe nonrecombining region. At a later stage, deletion ofnonfunctionalDNAfromwithintheSDRmayleadtoadecreasein the physical size of the SDR.There is also evidence that the nonrecombining region canprogressively encroach ontheflanking regions ofthechromo-some so that it encompasses an increasingly greater propor-tion of the sex chromosome. This process is thought to bedriven by the recruitment of genes with differential selectivebenefits to the two sexes (sexually antagonistic genes) intothe SDR [2] (but see [3]). Extension of the SDR in this mannercan lead to the creation of ‘‘strata,’’ which are regions of theSDR that have become nonrecombining at different points inevolutionary time [4–7].Thegeneticmechanismofsexdeterminationalsoinfluenceshow the sex chromosomes evolve. In organisms in which sexis expressed in the diploid phase, such as most animals andland plants, one sex is heterogametic (XY or ZW), whereasthe other is homogametic (XX or ZZ). In these systems, onlythe Y or W contains nonrecombining regions because the Xand Z recombine in the homogametic sex. In some algae andbryophytes, the male and female sexes are genetically deter-mined after meiosis, during the haploid phase of the life cycle[8, 9]. This type of sexual system, termed UV to distinguish itfrom the XY and ZW systems described above [10], exhibitsspecificevolutionaryandgeneticpropertiesthathavenoexactequivalent in diploid systems. In UV systems, the female andmale SDR haplotypes function in independent, haploid, maleand female individuals, and, consequently, there is no hetero-zygous sex comparable to XY males or ZW females. Thisdifference between UV and XY/ZW systems should haveimportant implications for SDR evolution [8, 9]. In particular,the female U and the male V are expected to be undersimilar evolutionary pressures not only because they function