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Diversity and Phylogenetic Implications of Cscl Profiles From Molecular Phylogenetics and Evolution Vol. 17, No. 2, November, pp. 219–230, 2000 doi:10.1006/mpev.2000.0838, available online at http://www.idealibrary.com on Diversity and Phylogenetic Implications of CsCl Profiles from Rodent DNAs Christophe Douady,*,†,1 Nicolas Carels,*,‡ Oliver Clay,*,‡ Franc¸ois Catzeflis,† and Giorgio Bernardi*,‡,2 *Laboratoire de Ge´ne´ tique Mole´ culaire, Institut Jacques Monod, Tour 43, 2 Place Jussieu, F-75005 Paris, France; †E´ quipe Phyloge´ nie Mole´ culaire, Laboratoire de Pale´ ontologie, Institut des Sciences de l’E´ volution, UMR 5554/UA 327, CNRS, Universite´ de Montpellier II, Case 064, Place Euge` ne Bataillon, F-34095 Montpellier cedex, France; and ‡Stazione Zoologica Anton Dohrn, Villa Comunale, I-80121 Naples, Italy Received December 13, 1999; revised July 17, 2000 INTRODUCTION Buoyant density profiles of high-molecular-weight DNAs sedimented in CsCl gradients, i.e., composi- The long, compositionally homogeneous regions of tional distributions of 50- to 100-kb genomic frag- which mammalian genomes consist, the isochores ments, have revealed a clear difference between the (ӷ300 kb on average), belong to a small number of 3 murids so far studied and most other mammals, in- families. Within any isochore family, GC levels of 50- cluding other rodents. Sequence analyses have re- to 100-kb regions, or fragments, vary little (2–3% GC); vealed other, related, compositional differences be- yet, together these isochore families span a wide GC tween murids and nonmurids. In the present study, we range, from 30 to 60% (Macaya et al., 1976; Thiery et obtained CsCl profiles of 17 rodent species represent- al., 1976; Cuny et al., 1981; Bernardi et al., 1985; ing 13 families. The modal buoyant densities obtained reviewed in Bernardi, 1995, 2000). for rodents span the full range of values observed in A buoyant density profile of genomic fragments, ob- other eutherians. More remarkably, the skewness tained by analytical ultracentrifugation of total nu- -asymmetry, mean ؊ modal buoyant density) of the clear DNA to sedimentation equilibrium in CsCl den) rodent profiles extends to values well below those of sity gradients, yields the distribution of the GC levels other eutherians. Scatterplots of these and related of the fragments, since buoyant density and GC of DNA CsCl profile parameters show groups of rodent fami- are linearly related (Schildkraut et al., 1962). In the lies that agree largely with established rodent taxon- present work, with the knowledge of eukaryotic ge- omy, in particular with the monophyly of the Geomy- nomes acquired using sequence-specific ligands over oidea superfamily and the position of the Dipodidae three decades, we reexamine the potential of screening family within the Myomorpha. In contrast, while con- CsCl profiles of total nuclear DNA, without further firming and extending previously reported differences fractionation or satellite analysis, as a tool for deduc- between the profiles of Myomorpha and those of other ing and clarifying mammalian phylogenies. This ap- rodents, the CsCl data question a traditional hypoth- proach was extensively used in previous work (see esis positing Gliridae within Myomorpha, as does the Bernardi, 1995, 2000 for reviews). recently sequenced mitochondrial genome of dor- For comparisons between vertebrate species, the ma- mouse. Analysis of CsCl profiles is presented here as a jor Gaussian components provide a robust character- rapid, robust method for exploring rodent and other ization of a species’ genome. All studies so far indicate vertebrate systematics. © 2000 Academic Press that there exists an invariant compositional pattern of Key Words: DNA; phylogeny; ultracentrifugation; ge- a genome or species, independent of the presence or nomes; base composition; rodents; vertebrates; Euth- absence of satellite DNA and of molecular weight dif- eria; evolution. ferences among DNA samples, that can be defined in terms of the Gaussian components of the CsCl profile’s main band, excluding satellite DNA. It is the set of relative amplitudes (amounts of DNA) and GC con- 1 tents (or buoyant densities, ␳) of these major compo- Present address: Medical Biology Centre, Biology & Biochemis- try, Queen’s University, 97 Lisburn Road, Belfast BT9 7BL, North- ern Ireland. 3 Abbreviations used: GC, molar fraction of guanine and cytosine 2 To whom correspondence should be addressed. E-mail: in DNA; ␳, buoyant density; ␳0, modal buoyant density; ͗␳͘, mean [email protected]. buoyant density. 219 1055-7903/00 $35.00 Copyright © 2000 by Academic Press All rights of reproduction in any form reserved. 220 DOUADY ET AL. 3 nents. The compositional pattern of a species’ genome high modal buoyant densities (␳0 Ն 1.700 g/cm ), ap- is usually shown as a bar plot (see, e.g., Macaya et al., pears also to be shared by all Muridae. The fact that 1976; Bernardi et al., 1985; Cuny et al., 1981; Bernardi, the Geomyoidea also exhibit high values of this param- 1995) or, alternatively, as a set of partially overlapping eter may be an artifact of unusually high proportions of Gaussian curves (Bernardi, 2000). Identifying the sat- satellite DNA, such as are found in other taxa of this ellite DNA, finding the major components (i.e., calcu- superfamily (notably in kangaroo rats; see Hatch and lating the compositional pattern), and inferring the Mazrimas, 1974). Alternatively, it may indicate high relative numbers of genes in them are key steps in modal buoyant densities also of nonsatellite DNA in understanding a species at the genome level. this superfamily, which McKenna and Bell (1972) in- A compositional pattern’s overall shape can often be clude in the Myomorpha suborder together with the estimated directly from a total DNA CsCl profile, with- Muridae and the Gliridae. out additional satellite information or fractionation. The phylogeny of rodents is far from settled, as this Moreover, as the present study confirms in the case of group is remarkable for having gone through a rapid rodents, these CsCl profiles can furnish robust, rapidly radiation leading to a tremendous diversity of fossil obtainable, and potentially powerful information for and recent taxa (Hartenberger, 1994, 1998a,b). Given systematics at the higher taxon levels (families, super- the paucity of sequence data in many rodent families families, infraorders, and suborders). Similar analyses (but see Huchon et al., 1999; Robinson et al., 1997a, should also be possible for other orders. For example, and references therein) and the rather large homoplasy bats (Chiroptera) exhibit an intraordinal variability of of morphological data, an additional type of molecular CsCl buoyant densities that appears to correlate with character that could detect or confirm relationships taxonomy, for Megachiroptera (flying foxes) have con- among the higher taxa (families and above) would be a sistently lower modal buoyant densities (GC levels) valuable tool. Given the diversity, yet relatively recent than Microchiroptera (echolocating microbats) (Arrighi radiation, of rodents, this order appeared to be an ideal et al., 1972; Pettigrew and Kirsch, 1995). taxon in which to explore the uses of the CsCl profile as Previous studies of the compositional distributions of a contribution to taxonomy and eventually to phylog- DNA fragments and genes from eutherian genomes eny. We therefore obtained more species’ profiles from have revealed the existence of two distinct composi- a wide range of rodent families and, using this larger tional patterns, or classes of patterns: a general pat- taxonomic sample, compared the groups of taxa that tern, common to nonrodents and some rodents, and a they imply with established or traditional phylogenies. murid pattern. (A third pattern, characterizing We also wished to obtain a more precise picture of the Megachiroptera, may also exist, but additional data two classes of compositional pattern within the rodent are needed to confirm its existence.) Early studies of order and to determine whether the pattern of the the compositional structures of mammalian genomes murines is present in rodents other than Muroidea or showed that the two murine genera Mus and Rattus Myomorpha. had clear peculiarities compared to other commonly In previous work (Thiery et al., 1976; Macaya et al., studied eutherians (Thiery et al., 1976). Distinguishing 1976; Salinas et al., 1986; Sabeur et al., 1993), CsCl characteristics of murine genomes include a different profiles and/or compositional patterns were obtained isochore organization (Cuny et al., 1981; Salinas et al., for a total of 20 eutherian species spanning nine or- 1986), a narrower compositional distribution of coding ders. The present study shows results of analytical sequences and third codon positions (Mouchiroud et al., centrifugation experiments in CsCl density gradients 1988; Bernardi, 1995), less stringent DNA repair and for 17 additional rodent species. Together with the 8 maintenance (see Holliday, 1995, and references there- rodent species for which results were already avail- in), a faster rate of nucleotide substitution (Li and able, the collection of rodent profiles now comprises 24 Tanimura, 1987; Chang et al., 1994) and chromosomal genera, representing 19 families of living rodents. rearrangements (Viegas-Pequignot et al., 1986; Early rodent CsCl profiles that were published Graves, 1996), and less pronounced or absent hypom- (Walker, 1968; Hennig and Walker, 1970; Mazrimas ethylated CpG islands (Aı¨ssani and Bernardi, 1991a,b; and Hatch, 1972) are unfortunately unreliable
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