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Discovery of Tetraploidy in a Mammal the Red Viscacha Rat Is Unaffected by Having Double the Usual Number of Chromosomes

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Discovery of Tetraploidy in a Mammal the Red Viscacha Rat Is Unaffected by Having Double the Usual Number of Chromosomes brief communications Discovery of tetraploidy in a mammal The red viscacha rat is unaffected by having double the usual number of chromosomes. olyploidy, or having more than a pair of each type of chromosome, is con- abcedfg Psidered to be unlikely in mammals 1 9 because it would disrupt the mechanism of dosage compensation that normally inacti- vates one X chromosome in females1. Also, 10 18 any imbalance in chromosome number should affect the normal developmental 19 27 processes and therefore constitute an evolu- tionary end, as in triploid humans2. Nevertheless, genetic evidence indicates 28 36 that the red viscacha rat, Tympanoctomys 3 barrerae (Octodontidae) , is tetraploid. T. 37 SC 45 barrerae, which is a highly specialized desert rodent4, has the largest chromosome com- plement in mammals5 with a single XY sex- 46 50 10µm XY 10 µm chromosome system (Fig. 1). Although little is known about meiotic chromosome Figure 1 C-banded karyotype of a male Tympanoctomys barrerae Figure 2 Bright-field photomicrograph of sperm cells from differ- pairing in T. barrerae, the constant diploid from Mendoza, Argentina (4N4102; fundamental number of ent genera in the families Octodontidae and Abrocomidae. a, Tym- number found in 13 specimens examined at autosomal arms is 200). The karyotype includes 36 pairs of meta- panoctomys barrerae; b, Aconaemys fuscus; c, Octodon degus; three localities in Argentina indicates that centric to submetacentric chromosomes and 14 pairs of subtelo- d, Spalacopus cyanus; e, Octomys mimax; f, Octodontomys segregation occurs normally. centric autosomes. The X chromosome is the largest element, gliroides; g, Abrocoma bennetti. In mammals without excessive consti- present in two copies in females. The Y chromosome, which is tutive heterochromatin in their chromoso- medium-sized, is the only acrocentric element of the karyotype. situ hibridization) and genome organiza- mal complement, nuclear DNA content is Note that the marker chromosome pair of the family Octodontidae tion (by looking for single-dose genes and relatively constant, ranging from 6 to 8 (secondary constriction, SC), which has a band of interstitial hete- clusters of linked duplicated genes) of T. picograms of DNA (mean, 6.3 pg)6. Analy- rochromatin, is present in only two copies, not four, as would be barrerae should enable this tetraploidy in T. sis of somatic tissues by flow cytometry expected following a perfect duplication. barrerae to be verified and will provide new indicates that T. barrerae has a genome of insights into the mechanisms underlying 16.8 pg, which is twice the DNA content of between T. barrerae (26.153.8 mm) and dosage compensation, sex determination, its closest relatives (for example, 8.2 pg Abrocoma bennetti (22.353.5 mm) or regulation of gene expression and develop- and 7.6 pg for Octodontomys gliroides and Octodon lunatus (21.352.7 mm). ment in mammals. The role of whole- Octomys mimax, respectively) and of most The müllerian explanation for the rarity genome duplication in triggering evol- other mammals. of tetraploidy among animals with XY sex- utionary novelty is exemplified by this The huge genome of T. barrerae cannot chromosome systems emphasizes inviability unique tetraploid mammal3. be explained by an increased amount of or sterility resulting from an altered dosage- Milton H. Gallardo*, J. W. Bickham†, heterochromatin because it is restricted to sensitive regulatory mechanism8. Sex deter- R. L. Honeycutt†, R. A. Ojeda‡, the centromere region of chromosomes. mination in mammals depends on the N. Köhler* Furthermore, the diploid number in T. bar- testis-determining locus, but in the germ *Instituto de Ecología y Evolución, rerae is less than that would be expected line it is affected by dosage of X-chromo- Universidad Austral de Chile, (2N4112) from a simple duplication of the some-linked genes9. The fact that polyploid Casilla 567, Valdivia, Chile karyotype seen in its closest relatives, indi- cells have more than one active X chromo- e-mail: [email protected] cating that chromosomal material has been some indicates that the signal to initiate †Department of Wildlife and Fisheries Sciences, eliminated. inactivation through heterochromatization Texas A&M University, College Station, The size of the sperm head in mammals may be dependent on the critical X-to- Texas 77843, USA depends on its DNA content, as exemplified autosomal chromosome ratio. ‡Instituto Argentino de Investigación de Zonas by the abnormally large and diploid sperm If there is an evolutionary elimination of Áridas, Cricyt, GIB Conicet Casilla de Correo 507, of rabbits and bulls7. The enormous broad chromosomes, as we propose, then the X-to- 5500 Mendoza, Argentina and spatulate sperm head of T. barrerae autosome ratio should not depend on the 1. Orr, H. A. Am. Nat. 136, 759–770 (1990). (Fig. 2) is 14.1 (50.6) by 13.4 (50.5) whole set of autosomes, but rather on some 2. Niebuhr, E. Humangenetik 21, 103–125 (1974). micrometres in size, and gametic genome critical autosomes needed in only one copy 3. Gallardo, M. H. in Chromosomes Today Vol 12 (eds Henríques-Gil, estimates are consistent with somatic esti- of the gamete. Thus, the disomic condition N., Parker, J. S & Puertas, M. J.) 347–365 (Chapman & Hall, 5 London, 1997). mates (Octomys mimax, 4.32 0.25 pg; of the X chromosome in female T. barrerae is 4. Ojeda, R. A. et al. J. Arid Environ. 41, 443–452 (1999). Spalacopus cyanus, 3.5450.27 pg; T. bar- either sufficient or possibly the only means 5. Contreras, L. C., Torres-Mura, J. C. & Spotorno, A. E. rerae, 9.250.72 pg). by which the tetraploid can escape arrested Experientia 46, 506–508 (1990). 6. Vinogradov, A. E. Cytometry 31, 100–109 (1998). As would be expected in a tetraploid gonadal development. This idea is support- 7. Ferrari, M. R., Spirito, S. E., Giuliano, S. M. & Fernández, H. A. organism, significantly larger somatic-cell ed by the inviability or infertility that affects Andrologia 30, 85–89 (1998). diameters were recorded. A highly signifi- human triploids, who do not have enough 8. Müller, H. Am. Nat. 59, 346–353 (1925). cant paired t-test (P*0.001) supported the diploid cells to undergo meiosis10. 9. Parkhurst, S. M. & Meneely, P. M. Science 264, 924–932 (1994). idea that there was a difference in the maxi- Investigation of the chromosomal archi- 10. Ohno, S., Kittrell, W. A., Christian, L. C., Stenius, C. & Witts, G. A. mum diameter of liver cells (N4150) tecture (by studying meiotic pairing and in Cytogenetics 2, 42–49 (1963). NATURE | VOL 401 | 23 SEPTEMBER 1999 | www.nature.com © 1999 Macmillan Magazines Ltd 341.
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