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Coexistence of Y, W, and Z Sex Chromosomes in Xenopus Tropicalis

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Coexistence of Y, W, and Z Sex Chromosomes in Xenopus Tropicalis Coexistence of Y, W, and Z sex chromosomes in Xenopus tropicalis Álvaro S. Rocoa, Allen W. Olmsteadb,1, Sigmund J. Degitzb, Tosikazu Amanoc, Lyle B. Zimmermanc, and Mónica Bullejosa,2 aDepartment of Experimental Biology, Faculty of Experimental Sciences, University of Jaén, Las Lagunillas Campus S/N, 23071 Jaén, Spain; bMid-Continent Ecology Division, Environmental Protection Agency, Duluth, MN 55804; and cDivision of Developmental Biology, Medical Research Council-National Institute for Medical Research, London, NW7 1AA, United Kingdom Edited by David C. Page, Whitehead Institute, Cambridge, MA, and approved July 1, 2015 (received for review March 28, 2015) Homomorphic sex chromosomes and rapid turnover of sex-determin- (3, 16, 17). Nevertheless, not all sex chromosomes are morpho- ing genes can complicate establishing the sex chromosome system logically distinct. This lack of differentiation does not always in- operating in a given species. This difficulty exists in Xenopus tro- dicate a recent origin of the sex chromosomes, as is the case in picalis, an anuran quickly becoming a relevant model for genetic, ge- ratite birds and boid snakes (18, 19). Two hypotheses have been nomic, biochemical, and ecotoxicological research. Despite the recent proposed to explain the lack of differentiation between some pairs interest attracted by this species, little is known about its sex chromo- of sex chromosomes: (i) occasional recombination between them, some system. Direct evidence that females are the heterogametic sex, as could happen in sex-reversed individuals (20), and (ii)frequent as in the related species Xenopus laevis, has yet to be presented. turnover of sex chromosomes because of rapid changes of sex- Furthermore, X. laevis’ sex-determining gene, DM-W, does not exist determining genes, preventing sex chromosome differentiation (21). in X. tropicalis, and the sex chromosomes in the two species are not Amphibians present genetic sex determination (GSD), with X. tropicalis’ homologous. Here we identify sex chromosome system temperature affecting sex differentiation in some species of the i ii by integrating data from ( ) breeding sex-reversed individuals, ( )gy- genera Pleurodeles, Hynobius, Bufo, and Rana and artificial iii iv nogenesis, ( ) triploids, and ( ) crosses among several strains. Our polyploids of the genus Xenopus (11, 22, 23). Despite ubiquitous results indicate that at least three different types of sex chromosomes GSD, the sex chromosome pair has been identified in only about exist: Y, W, and Z, observed in YZ, YW, and ZZ males and in ZW and 4% of analyzed species (24), not because of the lack of cyto- WW females. Because some combinations of parental sex chromo- logical studies [more than 25% of known Anura taxa have been somes produce unisex offspring and other distorted sex ratios, under- karyotyped (25, 26)], but because amphibian sex chromosomes standing the sex-determination systems in X. tropicalis is critical for are usually homomorphic (25). developing this flexible animal model for genetics and ecotoxicology. The diploid pipid frog Xenopus tropicalis has become an impor- tant model for developmental biology, genetics, evolutionary sex chromosomes | sex determination | sex reversal | gynogenesis | genomics, and ecotoxicology, but little is known about its sex Xenopus tropicalis chromosome system or mechanism of sex determination. All spe- cies from the genus Xenopus have homomorphic sex chromosomes ex chromosomes are unique karyotype features present only (27), including Xenopus laevis (28). However, breeding sex-reversed Sin species with genetic sex determination. They originate animals shows that females are the heterogametic sex in X. laevis from autosomes when a gene/locus assumes the sex-determining (29–31). Thus, estradiol treatment during development results in role either by acquisition of a sex-specific trigger or by gene sex-reversed genetically male, phenotypically female animals, which dosage effects on gonadal differentiation (1). Two main sex produce all-male offspring when mated to normal untreated males. chromosome systems can be found in vertebrates with genetic sex determination: XX/XY (in which males are heterogametic) Conversely, sex-reversed females obtained by exposure to grafts of and ZZ/ZW (with heterogametic females). Nevertheless, sex chromosomes are extraordinarily variable, and other combina- Significance tions also can be found, ranging from female heterogamety with 00/0W or ZZ/Z0 sex chromosomes (2, 3) to male heterogamety As in most amphibians, sex chromosomes of the model species with XX/X0 sex chromosomes (3). Furthermore, complex XY Xenopus tropicalis are homomorphic, complicating identification and ZW systems are possible when fusions, fissions, and trans- of the heterogametic sex. Using genetic approaches, we have locations between sex chromosomes and autosomes take place proved the existence of three types of sex chromosomes (Y, W, (e.g., X1X2Y, XY1Y2,orZ1Z2W) (for a review see ref. 1). and Z), defining three kinds of males (YZ, YW, and ZZ) and two Among vertebrates, amphibians, reptiles, and fish show remark- kinds of females (ZW and WW). The existence of both male and able variation in sex-determining mechanisms and sex chromosome female heterogametic individuals in one species is an extremely systems, not only between closely related species but even within rare situation in nature, because some sex chromosome combi- species. Taxa have been described with environmental sex determi- nations produce offspring with sex ratios different from 1:1. Thus, nation and cryptic sex chromosomes in reptiles (4), multiple sex parental sex chromosomes must be taken into account when X tropicalis chromosomes and polyfactorial sex determination in amphibians and . is used in multigeneration genetic studies or in eco- fishes (5–7), and frequent transitions between ZZ/ZW and XX/XY toxicological assays of endocrine disruptors with gender effects. sex chromosome systems in related species (8–11), with the extreme Author contributions: Á.S.R., A.W.O., S.J.D., L.B.Z., and M.B. designed research; Á.S.R., example of Rana rugosa, in which both sex chromosome systems are A.W.O., T.A., L.B.Z., and M.B. performed research; Á.S.R., A.W.O., S.J.D., L.B.Z., and M.B. differentiating independently in different populations (12). analyzed data; and Á.S.R., L.B.Z., and M.B. wrote the paper. It has been proposed that sex chromosomes differentiate when a The authors declare no conflict of interest. sex-determining region accumulates sexually antagonistic alleles, This article is a PNAS Direct Submission. favoring suppression of recombination (13). Nonrecombining regions See Commentary on page 10575. of sex-specific chromosomes (Y and W) degenerate progressively, 1Present address: Bayer CropScience, Research Triangle Park, NC 27709. leading eventually to cytogenetically distinct heteromorphic sex 2To whom correspondence should be addressed. Email: [email protected]. chromosomes (14, 15). In the most extreme cases, the Y or W This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. chromosome is lost entirely, resulting in the X0 and Z0 systems 1073/pnas.1505291112/-/DCSupplemental. E4752–E4761 | PNAS | Published online July 27, 2015 www.pnas.org/cgi/doi/10.1073/pnas.1505291112 Downloaded by guest on September 26, 2021 testicular tissue produce offspring with a female:male sex ratio of Table 1. Sex ratios observed in clutches after different PNAS PLUS 3:1 (30). Among the female offspring from these sex-reversed fe- treatments with synthetic estrogens “ ” males, one third were predicted to be WW superfemales, confirmed Strain Estrogen Dose, μg/L No. females No. males by crosses to normal males resulting in all-female clutches (31). The only sex-determining gene identified in amphibians to golden EE2 0.640 24* 0 † date is the DM-W gene from X. laevis (32). This gene is located (N/ICF1)IC β-Estradiol 10 40 2 on the W chromosome of this species (32, 33), confirming the (N/ICF1)IC β-Estradiol 50 14‡ 0 female heterogamety previously demonstrated by sex-reversal Total 78 2 experiments. However, DM-W is present in only some Xenopus EE2, ethynylestradiol. species and not in X. tropicalis or other amphibians (34). *Females identified in three spawns (n = 8 each). † SEE COMMENTARY Genetic markers linked to the X. tropicalis sex-determining All males with small testes. ‡ locus were identified in an amplified fragment-length polymor- Some females were sterile. phism study (35). These markers largely place to sequence scaf- folds that genetically map to the short arm of linkage group 7 (chromosome 7) (36, 37). (i.e., WW) were mated with control males. Consistent with a Although it has been proposed that X. tropicalis’ sex chromosome maternal WW genotype, the offspring were all female, indicating system is similar to that of X. laevis (33, 35, 36), experimental support that these matings were ♀ WW × ♂ ZZ = ♀ ZW. For a pedigree forthishypothesisislimited.Here we provide the first (to our of the sex-reversal experiment, see Figs. S1 and S2. knowledge) description of the sex chromosome system of X. tropicalis, integrating data from (i) breeding sex-reversed individuals, (ii)gy- Sex of Gynogenenetic Offspring. Production of viable diploid ani- nogenesis (both gynogenetic diploids and completely homozygous mals derived solely from the maternal genome, or gynogenesis, double haploids), (iii) triploids, and (iv) crosses among several labo- provides an independent method for analyzing
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