Journal of Heredity Advance Access originally published online on June 30, 2005
Journal of Heredity 2005 96(5):485-493; doi:10.1093/jhered/esi080
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Genome Sizes in Afrotheria, Xenarthra, Euarchontoglires, and Laurasiatheria
From the Laboratorio di Biologia dello Sviluppo e Centro di Eccellenza di Biologia Applicata, Università di Pavia, Pavia, Italy (Redi and Garagna); Windmühlenberg 6, Langwedel, Germany (Zacharias); Instituto de Biologia Cellular, Centro de Investigaciones en Reproduccion, Universidad de Buenos Aires, Buenos Aires, Argentina (Merani); Departamento de Estudios Ambientales, Universidad Simon Bolivar, Caracas, Venezuela (Oliveira-Miranda and Aguilera); Dipartimento di Medicina Sperimentale, Università di Parma, Parma, Italy (Zuccotti); and Dipartimento di Biologia Animale e dell'Uomo, Università di Roma La Sapienza, Roma, Italy (Capanna)
Address correspondence to C. A. Redi at the address above, or e-mail: carloalberto.redi{at}unipv.it.
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Abstract |
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Topical literature and Web site databases provide genome sizes for
4,000 animal species, invertebrates and vertebrates, 330 of which are mammals. We provide the genome size for 67 mammalian species, including 51 never reported before. Knowledge of genome size facilitates sequencing projects. The data presented here encompassed 5 Metatheria (order Didelphimorphia) and 62 Eutheria: 15 Xenarthra, 24 Euarchontoglires (Rodentia), as well as 23 Laurasiatheria (22 Chiroptera and 1 species from Perissodactyla). Already available karyotypes supplement the haploid nuclear DNA contents of the respective species. Thus, we established the first comprehensive set of genome size measurements for 15 Xenarthra species (armadillos) and for 12 house-mouse species; each group was previously represented by only one species. The Xenarthra exhibited much larger genomes than the modal 3 pg DNA known for mammals. Within the genus Mus, genome sizes varied between 2.98 pg and 3.68 pg. The 22 bat species we measured support the low 2.63 pg modal value for Chiroptera. In general, the genomes of Euarchontoglires and Laurasiatheria were found being smaller than those of (Afrotheria and) Xenarthra. Interspecific variation in genome sizes is discussed with particular attention to repetitive elements, which probably promoted the adaptation of extant mammals to their environment.
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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The word genome was coined in 1920 by Hans Winkler (1877–1945) while he was studying parthenogenesis in animals and plants. He defined genom (German spelling) as the haploid set of chromosomes and referred to the hypothesis that they are the sole carriers of hereditary factors. Today, the term is used in two distinct ways to indicate either the total number of genes or the whole amount of nuclear DNA. Considering both Winkler's definition and the fact that in the majority of organisms, only a small fraction of DNA comprises coding genes, we prefer for the definition of the total amount of DNA.
Early cytogeneticists quantified genomes by analyzing the partition in chromosomes that were counted in cytological preparations. However, the majority of nuclei remain in interphase, but the development of microphotometry allowed DNA measurements throughout the cell cycle. Thus, Hewson Swift introduced the C-value as a shortcut for any (haploid) genome. His first paper on animal nuclei, written for his PhD dissertation, discussed two competing ideas: Vendrely and Vendrely (1948) had proposed a hypothesis about DNA constancy, whereas Schrader and Leuchtenberger (1949) emphasized variability after they had recorded different DNA content in cell nuclei of the same species. In contrast to both positions, Swift (1950a) distinguished "DNA classes," which could increase by a factor of two from a fundamental class for a given species. Swift (1950b) expanded his discovery and showed that Feulgen DNA in corn nuclei was distributed in 1C, 2C, 4C, 8C, and 16C levels. He observed the DNA content 1C only at the end of meiosis (Greilhuber et al. 2005).
Genomes vary in size. This realization came from the pioneers of microphotometry shortly before the structure of DNA was discovered (Mandel et al. 1951; Marshak and Marshak 1953; Mirsky and Ris 1951; Swift and Kleinfeld 1953; Vendrely and Vendrely 1948).
The recognition that genome sizes (GS) are widely distributed prompted the formulation of the C-value paradox (Cavalier-Smith 1985; Thomas 1971). The most popular ideas are that GS is neither related to gene numbers nor to morphologic complexity, even though Van Nimwegen (2003) suggested scaling laws in the functional content of genomes in relation to the design of organisms. The completion of the euchromatic sequence of the human genome is an instructive example, resulting in some 20–25,000 protein-coding genes that represent less than 2% of all sequences (IHGSC 2004). The identification of repetitive sequences has only partially resolved the C-value paradox.
In the present study we evaluated the GS of several mammals of particular interest for comparative genomics (Hedges and Kumar 2002) and molecular phylogeny. Particularly, we focused on the whole spectrum of mice actually used in biomedical research, on the Xenarthra and the Chiroptera. From the first group, only the GS of the house mouse, Mus (musculus) domesticus, appears in databases. In current databases the Xenarthra are represented by only one species, the ant-eater, Myrmecophaga tridactyla, whereas the Afrotheria are represented just by the aardvark, Orycteropus afer.
Recent molecular studies (Delsuc et al. 2002; Madsen et al. 2001; Murphy et al. 2001, 2004) divide placentals into the Southern Hemisphere clades Afrotheria (elephants, hyraxes, aardvarks) and Xenarthra (sloths, ant-eaters, armadillos), opposite to the monophyletic Boreoeutheria in the Northern Hemisphere, which are composed of the Laurasiatheria clade (cetaceans, carnivores, bats) and the Euarchontoglires clade (rodents, lagomorphs, and primates). Statistical tests identified three early divergences with almost equal likelihood; these are a basal Afrotheria hypothesis, an Afrotheria plus Xenarthra alternative, and a basal Xenarthra hypothesis.
The available data and those we evaluated speak well for a general evolutionary tendency toward smaller GS in Boreoeutheria, in which the vast majority shows a GS around 3 pg. In contrast, the Xenarthra genomes have around 4.5 pg DNA, and the Afrotherian aardvark possesses 5.86 pg. We discuss possible mechanisms responsible for changes in GS. Quantitative variation of noncoding DNA sequences might not only obey intrinsic properties but could also be triggered by environmental signals. The resulting GS variations display nucleotypic effects in cell functions, and the organisms in question are exposed to natural selection forces. Such a scenario could render less enigmatic to understand the panoply of GS in mammals.
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Materials and Methods |
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Mammals
This investigation of nuclear DNA contents comprised 5 metatherian and 62 eutherian mammals. Most of the animals were caught in the wild using live traps at several localities in Argentina and Venezuela during the period 2000–2003. They were released after donating a drop of peripheral blood. Coordinates of the collection places are available on request. The zoos of Buenos Aires and Caracas gave blood smears from Priodonte maximus and Tapirus terrestris, respectively. Michael Potter (National Cancer Institute, Bethesda, MD) provided samples of Mus caroli, M. castaneus, M. cervicolor, M. cookii, M. spicilegus (also named M. hortulanus), M. molossinus, and M. spretus. The other Mus species came from animals housed at the Dipartimento di Biologia Animale, University of Pavia (Italy). Our intention was to use two slides for each of two animals per species, but only one animal was available from Marmosops fuscatus, Cabassous centralis, Dasypus kappleri, Priodonte maximus, Zaedyus pichiy, and Oecomys concolor.
Feulgen Procedure
Air-dried specimens were fixed in 10% formaldehyde aqueous solution for 20 min. The Feulgen reaction included hydrolysis in 5 M HCl at room temperature for 60 min and staining with Schiff's reagent (basic fuchsin; BDH) for 45 min. Several batches had to be processed, therefore it was important that each batch comprised slides bearing DNA standards. The standards were erythrocytes of the chicken (Gallus gallus) and sperms and lymphocytes of M. domesticus with 2.54, 3.4, and 6.8 pg nuclear DNA, respectively. Weak fading and minor sensitivity to DNA base composition are advantages of Feulgen staining.
Microphotometry
Twenty-five nuclei of lymphocytes and monocytes were measured from each slide. Thus, most samples had 100 nuclei, so that both interindividual and intraindividual (technical) variability was taken into account. Six samples were limited to 50 nuclei when only one animal was available (see previous description).
Nuclear DNA contents were recorded with a scanning microscope photometer 03 and the APAMOS program (Zeiss). The wavelength for maximum absorbance was determined at 550 ± 5 nm instead of expected 560 nm. A planapochromat 100x objective (n.a. 1.3) opened the measuring diameter to 0.5 µm and the illuminated field to 10 µm, both in the plane of the specimen. Therefore, scanning steps were set to 0.5 mm in both dimensions and for all measurements.
Open Access Databases
Several Web sites host databases on or providing links to animal (and plant) genome resources (last visit December 15, 2004).
- Animal Genome Size Database offers C-values from about 1,300 invertebrates and 2,500 vertebrates; it is maintained by Ryan Gregory, University of Guelph, Canada: www.genomesize.com.
- Cancer Genomics and a Mouse Expression Atlas are provided (among others) from the British Columbia Genome Sciences Centre, directed by Marco Marra and under the auspices of the BC Cancer Agency, Vancouver, Canada: www.bcgsc.ca.
- DBA Mammalian Genome Size Database has 237 data sets managed by Daniele Formenti, Dipartimento di Biologia Animale, Pavia University, Italy: www.unipv.it/webbio/dbagsdb.htm.
- DOGS, the Database of Genome Sizes covers 301 organisms; it is directed by Sören Brunak, Center for Biological Sequence Analysis, Technical University of Denmark in Lyngby: www.cbs.dtu.dk/databases/dogs.
- EBI, the European Bioinformatics Institute, gives access to completed genomes and genome shotgun sequences; it is at Wellcome Trust Genome Campus, Hinxton, Cambridge, UK: www.ebi.ac.uk/genomes.
- ENSEMBL is a joint project between the EBI, Cambridge, and the Sanger Institute, London, to develop a software system for automatic annotation on metazoan genomes: www.ensembl.org.
- GOLD: the Genomes Online Database represents a Web resource for genome projects worldwide referring to 463 eukaryotic genomes; it is kept by Nikos C. Kyrpides, Lawrence Berkeley National Laboratory, Berkeley, CA: www.genomesonline.org.
- HGMP, the Human Genome Mapping Project provides links to genome databases; it is managed by the Rosalind Franklin Centre for Genomics Research, Medical Research Council, Hinxton, Cambridge, UK: www.hgmp.mrc.ac.uk/genomeweb.
- JGI, the Joint Genome Institute, is operated by the University of California for the U.S. Department of Energy. It offers a Genome Portal to download sequences; details on human chromosomes 5, 16, 19; and entry to the Evolutionary Genomics Department. JGI Production Genomics Facility, Walnut Creek, CA: www.jgi.doe.gov.
- KEGG, the Kyoto Encyclopedia of Genes and Genomes, provides (among other things) a database about genome projects with 243 entries; it was set up by Minoru Kanehisa at Bioinformatics Center, Institute for Chemical Research, Kyoto University, Tokyo: www.genome.ad.jp/kegg.
- Plant DNA C-values Database was initiated by Michael Bennett and Ilja Leitch and got release 3.0 in December 2004. Royal Botanic Gardens Kew, Richmond, Surrey, UK: www.rbgkew.org.uk/cval.
- VEGA, the Vertebrate Genome Annotation browser, makes its focus on human, mouse, and zebrafish; it is operated by the Wellcome Trust Sanger Institute, London: www.vega.sanger.ac.uk.
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Results |
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We measured the nuclear DNA contents of 5 metatherian and 62 eutherian mammals (Table 1). Their GS were calculated in picograms of 1C DNA and also converted into Mbp using a factor of 978 (Dolezel et al. 2003). In parentheses, 16 already available GS were added from databases (Material and Methods). Our estimates agree with 14 of these data points, but there were remarkable differences for Didelphis marsupialis (21%) and Mus poschiavinus (23%).
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Subclass Metatheria
Five species of opossums, family Didelphidae, could be investigated. The smallest GS of 2.85 pg DNA was found in M. fuscatus, whereas the largest, 5.22 pg, came from Monodelphis brevicaudata. Thus, the genomic range for pouched mammals was expanded, because the 26 species already studied had occurred between 3.0 and 4.9 pg DNA. Their modal GS was more than the average, slightly above 3 pg, as known for mammals in general.
Subclass Eutheria
Xenarthra. The order of extra-jointed animals, endemic to Central and South America, had been represented in the databases only by the giant ant-eater Myrmecophaga tridactyla. Its GS had been given 4.15 pg DNA, for which the present measurement was 4.49 pg. Tamandua tetradactyla is another representative of the Myrmecophagidae, which showed here 4.11 pg DNA. The first record for three-toed sloths, family Bradypodidae, was 4.23 pg from Bradypus variegatus; it lies in the order of the Myrmecophagidae. In addition, we considered 12 species of armadillos, family Dasypodidae, which ranged between 3.98 pg in Cabassous centralis and 5.76 pg in Dasypus sabanicola. Thus, their GS appeared much larger than the modal value known for mammals.
Rodentia. This order has the largest number of species. Their GS scattered to a greater extent than those of the other orders in consideration. Heteromys anomalus and Microryzomys minutus displayed the smallest genomes of 2.77 pg and 2.78 pg, whereas the largest, 6.21 pg and 6.25 pg, were found in Proechymis guairae and P. trinitatis, respectively. However, variability was less evident at the level of families and appeared particularly low in Muridae.
We measured the GS of several house-mouse species, of which 10 were unknown. The values reported hitherto were from M. musculus and M. poschiavinus. The latter refers to the house mouse from the Poschiavo valley in Switzerland. But this naming should be avoided, because these animals represent just one of the many variants from Robertsonian chromosomes within the wild-living short-tailed mice in Western Europe (Redi and Capanna 1988). The taxonomy of the house mouse species assigned the poschiavinus animals to M. musculus domesticus (Marshall and Sage 1981); we prefer the abridged version M. domesticus. Furthermore, M. musculus musculus—or better, M. musculus—is the correct term for the wild-living long-tailed mice in Eastern Europe. Unfortunately, the literature does not completely comply with Marshall's and Sage's suggestions. GS databases likewise indicated M. musculus, even though the animals were M. domesticus. Such incorrect terminology puts a risk to biomedical research and genomic studies.
The value we estimated for poschiavinus animals was 3.22 pg DNA. This is different from the former report of 3.97 pg, but rather close to 3.35 pg for M. domesticus. The largest murine genome of 3.68 pg DNA turned out in our coherent approach with M. spretus. Its GS exceeded that of other mice, probably due to the amplification of minor satellite sequences (Garagna et al. 1993).
Perissodactyla. Tapirus terrestris, the South American tapir, is the third species in this order, from which the GS became known. Its value of 3.78 pg DNA is situated between 3.15 pg for the horse and 4.12 pg for the donkey. The database presentation of even-toed ungulates surpasses that of perissodactyls, because most of the 18 GS for Artiodactyla have been obtained from domestic animals.
Chiroptera. The GS databases hitherto included 50 bat species. This investigation added 12 original records that confirmed the minor variability of GS already known for this order. Myotis keaysi showed the minimum GS with 2.34 pg, whereas Carollia brevicauda the maximum with 2.98 pg. The majority of bat values ranged around 2.6 pg DNA.
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Discussion |
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Sizing Mammalian Haploidy
The research community experiences and produces a growing need to analyze new genomes. Sequencing projects, however, demand not only hefty budgets but also a wide overview on the breadth of genomic capacities.
Consider the practical interest in the correct GS of a species. The nine-banded armadillo, Dasypus novemcinctus, was selected for sequencing, and the BAC library now under construction has been based on a presumptive GS of 3.0 pg DNA (www.genome.gov). However, we estimated a much larger GS of 5.41 pg. Knowledge of GS facilitates a suitable and efficient sequencing strategy. It is of particular relevance considering the frequency with which genomes are entering sequencing projects (www.genomesonline.org); these were 76 just from July 29 to October 6, 2003, and 296 from then to June 11, 2004.
Knowledge about the extent of GS conservation and divergence will help unravel the genetic and evolutionary mechanisms that shape genomes. Therefore, we attempted to fill in some gaps in the mammalian GS database. This enterprise encompassed 67 species from Metatheria as well as Eutheria, where hitherto a paucity of data prevailed (Table 1).
Recent molecular data split the placental orders into four phylogenetic clades. Afrotheria, and Xenarthra occupy basal positions, followed by the Boreoeutheria, which embrace Euarchontoglires and Laurasiatheria (Delsuc et al. 2002; Madsen et al. 2001; Murphy et al. 2001, 2004). The actually known data for 373 eutherian mammals attribute the largest genomes to the aardvark (Orycteropus afer, Afrotheria) and to Xenarthra (Figure 1). Both types of results shall converge by the assumption that there has been a shift toward smaller genomes during the transition of basal clades to the Boreoeutheria that conquered the Northern Hemisphere. This suggestion requires extensive exploration of Afrotherian genomes (Fronicke et al. 2003; Svartman et al. 2004) .
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Compacted Genomes
The genome of the verspertilionid Myotis capaccinii is composed of just 1.9 pg DNA (Capanna and Manfredi Romanini 1971). Here, an additional 21 bat species were found to possess rather small GS (<3 pg; Table 1); thus, they represent valuable models for comparative genetics to find essential features.
Because the GS correlates positively with nuclear and cellular volumes, small genomes appear well adapted to the metabolic requirements for flight (Hughes and Hughes 1995). This correlation holds also for birds, where larger genomes were risky for extinction (Vinogradov 2004a) and continue only in running species (Tiersch and Wachtel 1991). Bats achieve their small genomes thanks to a minimum of repetitive DNA elements (Van den Bussche et al. 1995). This characteristic might facilitate the identification of regulatory sequences in noncoding DNA.
An extreme example of small GS is the tetraodontoid fish Fugu rubripes. Its 1C content of 0.41 pg DNA was estimated to possess nearly the same number of genes as humans (www.genome.jgi-psf.org/fugu). Although most of the human genome is made up of noncoding DNA, the Fugu carries only a handful of giant genes containing long introns. Nevertheless, some 10% of sequences are repetitive. These findings suggest that even the smallest genomes need a minimum of repetitive DNA to correctly express genes responsible for complex functions. By engulfing a genome, these sequences may participate in the "eurygenic" system of gene regulation, which requires sectors of noncoding DNA (Vinogradov 2004b; Zuckerkandl and Hennig 1995).
Redundancy in Genomes
In the majority of mammals, protein-coding exons contribute merely 2% to the GS. The rest is composed in almost equal portions by repetitive DNAs and by unique sequences of mainly unknown function (Sogayar et al. 2004). Particularly the ubiquitous repetitive elements, cytologically detectable or not, account for varying C-values even among closely related taxa (John 1988; Manfredi Romanini 1985).
Despite earlier negative attributes, repetitive DNAs are nowadays not regarded as useless (Beaton and Cavalier-Smith 1999). They rather provide an efficient mechanism for genomic shuffling. Makalowski (2000) has bridged the difference of opinion by his concept of a genomic scrap yard, from which evolution may serve itself.
The long interspersed nucleotide element LINE-1 is an autonomous retroelement that makes up about 16% of the human genome. LINE-1 can jump to chromosomes with broken DNA strands and then slip into and repair the damage (Morrish et al. 2002).
Repetitive sequences contribute not only to GS variation (Petrov 2001; Vinogradov 1998), but also ensure the maintenance of a definite three-dimensional chromatin order, which is a prerequisite for its correct and efficient functioning (Cremer et al. 1993; Spector and Gasser 2003). Heterochromatin is an acknowledged stronghold of repetitive DNAs, which interact with surrounding sequences and nearby genes. Repetitive DNA sequences may serve as recombination hot spots or become part of protein coding regions. They have specific functions in dosage compensation, sister chromatid cohesion, and telomere maintenance. More general effects appear in the repression of gene activities, position effect variegation, DNA elimination, differential DNA endoreplication, and concurrent variations in GS (Grewal and Moazed 2003; Redi et al. 2001). In addition, when examining samples from many individuals of the same species, the amount of heterochromatin at specific loci may not be constant. The grasshopper Atractomorpha similis is an impressive example, in that all 10 chromosomes of the haploid set can be affected so that more than 250 cytotypes have been detected (John and King 1983). Such intraspecies heterochromatin polymorphisms are apparently without phenotypic expression.
We are challenged to deviate from a narrow gene-centered view, because coding sequences alone neither tell the whole story of life nor account for the organismal complexity. To understand genome functioning better, the linear genome map must be supplemented with studies on the epigenetic mechanisms of gene regulation and expression. The so-called nucleotypic effect allots a role to GS itself (Bennett 1972; Gregory 2001; Olmo et al. 1989; Olmo 2003); particularly considering the clear negative correlation with metabolic rates (Vinogradov 1998). We might also learn how genomic elements allow cross-talk between environmental signals and genomic receptors.
Genomic Ecology
Signal transduction networks convey information about extracellular and intracellular environments to the nucleus, while coordinated relocation of large DNA sections is feasible thanks to natural genetic engineering systems (Shapiro 1997). The rapid restructuring of the maize genome in response to the "genome shock" is a classical example, and ciliate macronuclear development is another. Furthermore, phytochrome-mediated shade-avoiding and light-seeking responses in flowering plants have been proven to be based on a family of regulatory multigenes in Arabidopsis thaliana (Callahan et al. 1997). Thus, repetitive DNA elements appeared as appropriate candidates for being the physical basis that couples the nucleus and its environment.
A recent example of such inside-outside cross-talk is the finding that human Alu element retrotransposition can be induced by exposure to the topoisomerase II inhibitor etoposide that is mediated in trans by endogenous LINEs (Hagan et al. 2003). Alu elements are quite abundant, accounting for about 10% of the human genome. The fact that retrotransposition can be induced by genotoxic stress supports the scenario of GS variations triggered by environmental signals.
Documented molecular mechanisms for amplification and dispersion throughout the genome comprise not only transposable elements (Kidwell 2002) but also illegitimate recombination, unequal crossing over, deletion, and duplication of larger genomic segments. These processes of DNA metabolism are capable of producing quantitative as well as qualitative rearrangements. They could prove to be key events in generating significant functional variability, which will be faced with selection in the Darwinian world.
When exploring new ecological niches, the outcome organism's GS variation must withstand examination of what might be likely to survive: the GS variation will be selected for new favorable physiological answers. At the risk of oversimplification, we suggest that the exons of a genotype plus the GS per se might be the new paradigm to explain, in a more comprehensive manner, the determination of a phenotype.
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Acknowledgments |
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Supporting grants: the bilateral project 55M-2002 (Italian MAE, Argentinian SETCIP) to C. A. Redi and M. S. Merani; the Proyecto Fonacit, Venezuela, no. 9800341 and the Italian COFIN 2003 to C. A. Redi and E. Capanna. Special thanks to M. G. Manfredi Romanini, Alessandro Minelli, Ettore Olmo, and Roscoe Stanyon for critical reading and helpful comments that greatly improved our manuscript.
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Footnotes |
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Corresponding Editor: Stephen O'Brien
Received January 28, 2005
Accepted March 15, 2005
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References |
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Aguilera M, Pérez-Zapata A, and Martino A, 1995 Cytogenetics and karyosystematics of Oryzomys albigularis (Rodentia, Cricetidae) from Venezuela Citog Cell Genetics 6944–49..
Baker RJ, 1967 Karyotypes of the bats of the family Phyllostomidae and their taxonomic implications SW Naturalist 12407–428..
Baker RJ, 1973 Comparative cytogenetics of the New World leaf-nosed bats (Phyllostomatidae) Period Biol 7537–45..
Baker RJ and Hsu TC, 1970 Further studies of the sex-chromosome system of the American leaf-nosed bats (Chiroptera:Phyllostomidae) Cytogenetics 9131–138..[Medline]
Baker RJ and Patton JL, 1967 Karyotypes and karyotypic variation of North American vespertilionid bats J Mammalogy 48270–286.[CrossRef]
Baker R, Haiduk MW, Robbins LW, Cadena A, and Koop BF, 1982 Chromosomal studies of South American bats and their systematics implicatons In: Mammalian Biology in South America. Special Publications Series, Pymatuning Laboratory of Ecology, vol 6. Pittsburgh, PA: University of Pittsburgh; 303–327.
Barroso CM and Seuanez H, 1991 Chromosome studies on Dasypus, Euphractus and Cabassous genera (Edentata: Dasypodidae) Cytobios 68179–196.[Medline]
Beath MM, Benirschke K, and Brownhill LE, 1962 The chromosomes of the ninebanded armadillo, Dasypus novemcinctus Chromosoma 1327–38.[ISI][Medline]
Beaton MJ and Cavalier-Smith T, 1999 Eukaryotic non-coding DNA is functional: evidence from the differential scaling of cryptomonal genomes Proc R Soc London B 2662053–2059.[Medline]
Benirschke K and Wurster DH, 1969 The chromosomes of the giant armadillo, Priodontes giganteus Geoffroy Acta Zool Pathol Antverpiensia 49125–130.
Bennett MD, 1972 Nuclear DNA content and minimum generation time in herbaceous plants Proc R Soc Lond B 181109–135.[Medline]
Callahan HS, Pigliucci M, and Schlichting CD, 1997 Developmental phenotypic plasticity: where ecology and evolution meet molecular biology BioEssays 19519–525.[CrossRef][ISI][Medline]
Capanna E and Manfredi Romanini MG, 1971 Nuclear DNA content and morphology of the karyotype in certain Paleartic microchiroptera Caryologia 24471–482.[ISI]
Capanna E, Gropp A, Winking H, Noack G, and Civitelli MV, 1976 Robertsonian metacentrics in the mouse Chromosoma 58341–353.[CrossRef][ISI][Medline]
Carvalho BD and Mattevi MS, 2000 (T2AG3)n telomeric sequence hybridization suggestive of centric fusion in karyotype marsupials evolution Genetica 108205–210.[CrossRef][ISI][Medline]
Cavalier-Smith T, ed 1985 The evolution of genome size Chichester: John Wiley.
Cremer T, Kurz A, Zirbel R, Dietzel S, Rinke B, Schroeck E, Speicher MR Mathieu U, Jauch A, Emmerich P, and others 1993 Role of chromosome territories in the functional compartmentalization of the cell nucleus In: DNA and chromosome Cold Spring Harbor Symp Quant Biol 58777–792.[ISI][Medline]
Delsuc F, Scally M, Madsen O, Stanhope MJ, De Jong WW, Catzeflis FM, Springer MS, and Douzery EJP, 2002 Molecular phylogeny of living Xenarthrans and the impact of character and taxon sampling on the placental tree rooting Mol Biol Evol 191656–1671.
Dolezel J, Barto J, Voglmayr H, and Greilhuber J, 2003 Nuclear DNA content and genome size of trout and human Cytometry 51127–128.[Medline]
Eisenberg JF, 1989 Mammals of the neotropics vol I: Panama, Colombia, Venezuela, Guyana, Suriname and French Guiana Chicago: University of Chicago Press.
Fronicke L, Wienberg J, Stone G, Adams L, and Stanyon R, 2003 Towards delineation of the ancestral eutherian genome organization: comparative genome maps of human and the African elephant (Loxodonta africana) generated by chromosome painting Proc R Soc Lond B 2701331–1340.[Medline]
Garagna S, Redi CA, Capanna E, Andayani N, Alfano RM, Doi P, and Viale G, 1993 Genome distribution, chromosomal allocation, and organization of the major and minor satellite DNAs in 11 species and subspecies of the genus Mus Cytogenet Cell Genet 64247–255.[ISI][Medline]
Gardner AL, 1977 Chromosomal variation in Vampiresia and a review on chromosomal evolution in the Phyllostomatidae (Chiroptera) Syst Zool 26300–318.
Gardner AL and O'Neill JP, 1969 The taxonomic status of Sturnira bidens (Chiroptera:Phyllostomidae) with note of its karyotype and life history Occ Pap Mus Zool LSU 381–8.
Gardner AL and Patton JL, 1976 Karyotype variation in Oryzomine rodents (Cricetidae) with comments of chromosomal evolution in the neotropical cricetine complex Occ Pap Mus Zool LSU 491–47.
Goldschmidt B and De Almeida JC, 1993 Cytogenetic studies in sloths (Bradypus variegatus) Rev Bras Genét 16939–948.
Gregory TR, 2001 Coincidence, coevolution, or causation? DNA content, cell size and the C-value enigma Biol Rev 7665–101.[Medline]
Greilhuber J, Dolezel J, Lysák MA, and Bennett MD, 2005 The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents Annals Bot 95255–260.
Grewal SI and Moazed D, 2003 Heterochromatin and epigenetic control of gene expression Science 301798–802.
Gropp A, Tettenborn U, and von Lehmann E, 1970 Chromosomenvariation vom Robertson'schen Typus bei der Tabakmaus, M. poschiavinus, und ihren Hybriden mit der Laboratoriumsmaus Cytogenet Cell Genet 99–23.
Hagan CR, Sheffield RF, and Rudin CM, 2003 Human Alu element retrotransposition induced by genotoxic stress Nat Genet 35219–20.[CrossRef][ISI][Medline]
Hedges SB and Kumar S, 2002 Vertebrate genomes compared Science 2971283–1285.[ISI][Medline]
Houck ML, Kingswood SC, and Kumamoto AT, 2000 Comparative cytogenetics of tapirs, genus Tapirus (Perissodactyla, Tapiridae) Cytogen Genome Res 88110–115.[CrossRef]
Hsu TC, 1965 Chromosomes of two species of anteaters Mamm Chrom Newslett 15108–109.
Hsu TC and Benirschke K, various years An atlas of mammalian chromosomes, volumes 1 (1967), 2 (1968), 3 (1969), 4 (1970), 5 (1971), 6 (1971), 8 (1974), 10 (1977) Berlin, Heidelberg, New York: Springer.
Hughes AL and Hughes MK, 1995 Small genomes for better flyers Nature 377391.[Medline]
IHGSC (International Human Genome Sequencing Consortium), 2004 Finishing the euchromatic sequence of the human genome Nature 431931–945.[CrossRef][Medline]
John B, 1988 The biology of heterochromatin In: Heterochromatin (Verma RS, ed). Cambridge: Cambridge University Press; 1–147.
John B and King M, 1983 Population cytogenetics of Atractomorpha similis. I: C band variation Chromosoma 8857–68.[CrossRef]
Jorge W, 1981 Estudo cromossômico de algumas espécies da ordem Edentata Tese de Livre-Docência a presentada ao Instituto Básico de Biologia Médica e Agrícola—UNESP, Botucatu.
Jorge W, Merrit DA, and Benirschke K, 1977 Chromosome studies in Edentata Cytobios 18157–172.
Kidwell MG, 2002 Transposable elements and the evolution of genome size in eukaryotes Genetica 11549–63.[CrossRef][ISI][Medline]
Madsen O, Scally M, Douady CJ, Kao DJ, DeBryk RW, Adkins R, Amrine HM, Stanhope MJ, De Jong WW, and Springer MS, 2001 Parallel adaptive radiations in two major clades of placental mammals Nature 409610–614.[CrossRef][Medline]
Makalowski W, 2000 Genomic scrap yard: how genomes utilize all that junk Gene 25961–67.[CrossRef][ISI][Medline]
Makino S, 1951 An atlas of the chromosome numbers in animals, 2d ed Ames: Iowa State College Press.
Manfredi Romanini MG, 1985 The nuclear content of desoxyribonucleic acid and some problems of mammalian phylogenesis Mammalia 49369–385.
Mandel P, Métais P, and Cuny S, 1951 Les quantités d'acide désoxypentose-nucléique par leucocyte chez diverses espèces de mammifères Compt Rend Acad Sci 2311172–1174.
Marshak A and Marshak C, 1953 Desoxyribonucleic acid in Arbacia eggs Exp Cell Res 5288–300.[CrossRef][ISI][Medline]
Marshall JT and Sage RD, 1981 The taxonomy of the house mouse In: The biology of the house mouse (Berry RJ, ed). London: Academic Press; 15–26.
Merrit DA, Low R J, and Benirschke K 1973 The chromosomes of Zaedyus pichi Mamm Chrom Newslett 14108–109.
Mirsky AE and Ris H, 1951 The desoxyribonucleic acid content of animal cells and its evolutionary significance J Gen Physiol 34451–462.
Morrish TA, Gilbert N, Myers JS, Vincent BJ, Stamato TD, Taccioli GE, Batzer MA, and Moran JV, 2002 DNA repair mediated by endonuclease-independent LINE-1 retrotransposition Nat Genet 31159–165.[CrossRef][ISI][Medline]
Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryderk OA, and O'Brien SJ, 2001 Molecular phylogenetics and the origins of placental mammals Nature 409614–618.[CrossRef][Medline]
Murphy WJ, Pevzner PA, and O'Brien SJ, 2004 Mammalian phylogenomics comes of age Trends Genet 20631–639.[CrossRef][ISI][Medline]
Olmo E, 2003 Reptiles: a group of transition in the evolution of genome size and of the nucleotypic effect Cytogenet Genome Res 101166–171.[CrossRef][ISI][Medline]
Olmo E, Capriglione T and Odierna G 1989 Genome size evolution in vertebrates: trends and constraints Comp Biochem Physiol B 92447–453.[CrossRef][Medline]
Patton JL and Gardner AL, 1971 Parallel evolution of multiple sex-chromosome systems in the phyllostomatid bats, Carollia and Choeroniscus Experientia 27105–112.[CrossRef][ISI][Medline]
Pérez-Zapata A, Reig OA, Aguilera M, and Ferrer A, 1986 Cytogenetics and karyosystematics of South American oryzomine rodents (Cricetiade: Sigmodontinae). I. A species of Oryzomys with a low chromosome number from morthern Venezuela Z Saugëtierkunde 5368–378.
Pérez-Zapata A, Vitullo AD, and Reig OA, 1987 Karyotypic and sperm distinction of Calomys hummelinki from Calomys laucha (Rodentia:Cricetidae) Acta Cient Venez 3690–93.
Pérez-Zapata A, Aguilera M, Ochoa J, and Soriano M, 1996 Citogenética de rodepres de altura: Microryzomys minutus y Neacomys tenuipes Acta Cientìfica Venezolana 4776.
Petrov DA, 2001 Evolution of genome size: new approaches to an old problem Trends Genet 1723–28.[CrossRef][ISI][Medline]
Redi CA and Capanna E, 1988 Robertsonian heterozygous in the house mouse and the fate of their germ cells In: The cytogenetics of mammalian autosomal rearrangements (Daniel A, ed). New York: Alan Liss; 315–359.
Redi CA, Garagna S, Zacharias H, Zuccotti M, and Capanna E, 2001 The other chromatin Chromosoma 110136–147.[ISI][Medline]
Reig OA, Tranier M, and Barros MA, 1979a Sur l'identificación chromosomique de Proechimys guyannensis Geoffroy 1803 et de Proechimys cuvieri Petter 1978 (Rodentia, Echimydae) Mammalia 4335–39.
Reig OA, Barros MA, Useche M, Aguilera M, and Linares OJ, 1979b The chromosome of spiny rats, Proechimys trinitatis, from Trinidad and eastern Venezuela (Rodentia, Echimydae) Genetica 51153–158.[CrossRef]
Reig OA, Aguilera M, Barros MA, and Useche M, 1980 Chromosomal speciation in a rassenkreiss of Venezuelan spiny rats (Genus: Proechimys, Rodentia, Echimydae) Genetica 52291–312.[CrossRef]
Saez FA, Drets ME, and Brum N, 1964 The chromosomes of the mulita (Dasypus hybridus): a mammalian edentate of South America In: Mammalian cytogenetics and related problems in radiobiology (Pavan C, ed). New York: Pergamon Press; 163–170.
Schmid M, Steinlein C, Feichtinger W, Schmidt M, Visbal R, and Fernàndez-Badillo A, 1992 An Intriguing Y chromosome in Heteromys anomalus (Rodentia, Heteromyidae) Hereditas 117209–214.[ISI][Medline]
Schrader F and Leuchtenberger C, 1949 Variation in the amount of desoxyribose nucleic acid in different tissues of Tradescantia Proc Natl Acad Sci USA 35464–468.
Shapiro JA, 1997 Genome organization, natural engineering and adaptive mutation Trends Genet 1398–104.[CrossRef][ISI][Medline]
Sogayar MC, Camargo AA, Bettoni F, and others 2004 A transcript finishing initiative for closing gaps in the human transcriptome Genome Res 141413–1423.
Spector DL and Gasser SM, 2003 A molecular dissection of nuclear function EMBO Reports 418–23.[CrossRef][ISI][Medline]
Svartman M, Stone G, Page JE, and Stanyon R, 2004 A chromosome painting test of the basal eutherian karyotype Chromosome Res 1245–53.[CrossRef][ISI][Medline]
Swift H, 1950a The desoxyribose nucleic acid content in animal nuclei Physiol Zool 23169–198.[Medline]
Swift H, 1950b The constancy of desoxyribose nucleic acid in plant nuclei Proc Natl Acad Sci USA 36643–654.
Swift H and Kleinfeld R, 1953 DNA in grasshopper spermatogenesis, oogenesis and cleavage Physiol Zool 26301–311.
Thomas CA, 1971 The genetic organization of chromosomes Ann Rev Genet 5237–256.[CrossRef][ISI][Medline]
Tiersch TR and Wachtel SS, 1991 On the evolution of genome size in birds J Hered 82363–368.
Van den Bussche RA, Longmire JL, and Baker RJ, 1995 How bats achieve a small C-value: frequency of repetitive DNA in Macrotus Mam Gen 6521–525.
Van Nimwegen E, 2003 Scaling laws in the functional content of genomes Trends Genet 19479–484.[CrossRef][ISI][Medline]
Vendrely R and Vendrely C, 1948 La teneur du noyau cellulaire en acide désoxyribonucléique à travers les organes, les individus et les espèces animales: Techniques et premiers résultats Experientia 4434–436.[Medline]
Vinogradov AE, 1998 Buffering: a possible passive-homeostasis role for redundant DNA J Theor Biol 193197–199.[CrossRef][ISI][Medline]
Vinogradov AE, 2004a Genome size and extinction risk in vertebrates Proc R Soc Lond B 2711701–1705.[Medline]
Vinogradov AE, 2004b Evolution of genome size: multilevel selection, mutation bias or dynamic chaos? Curr Opin Genet Dev 14620–626.[CrossRef][ISI][Medline]
Williams DF, 1978 Taxonomic and karyologic comments on small brown bats, genus Eptesicus, from South America Ann Carn Mus 47361–383.
Winkler H, 1920 Verbreitung und Ursache der Parthenogenesis im Pflanzen- und Tierreiche Jena: Gustav Fischer.
Yonenaga Y, 1968 Estudios cromossomicos em especies de Chiroptera Ciencia e Cutura 20172.
Zuckerkandl E and Hennig W, 1995 Tracking heterochromatin Chromosoma 10475–83.[ISI][Medline]
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