Molecular Biology and Evolution 18:132-143 (2001)
© 2001 Society for Molecular Biology and Evolution
ARTICLE |
Mitochondrial Versus Nuclear Gene Sequences in Deep-Level Mammalian Phylogeny Reconstruction
*Department of Biology, University of California at Riverside;
Department of Biological Sciences, University of Cincinnati;
Queen's University of Belfast, Biology and Biochemistry, Belfast, Ireland;
§Department of Biochemistry, University of Nijmegen, the Netherlands;
||Institute for Systematics and Population Biology, Amsterdam, the Netherlands;
¶Bioinformatics, SmithKline Beecham Pharmaceuticals, Pennsylvania
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Abstract |
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Both mitochondrial and nuclear gene sequences have been employed in efforts to reconstruct deep-level phylogenetic relationships. A fundamental question in molecular systematics concerns the efficacy of different types of sequences in recovering clades at different taxonomic levels. We compared the performance of four mitochondrial data sets (cytochrome b, cytochrome oxidase II, NADH dehydrogenase subunit I, 12S rRNA–tRNA–16S rRNA) and eight nuclear data sets (exonic regions of
-2B adrenergic receptor, aquaporin, ß-casein, 
-fibrinogen, interphotoreceptor retinoid binding protein, 
-casein, protamine, von Willebrand Factor) in recovering deep-level mammalian clades. We employed parsimony and minimum-evolution with a variety of distance corrections for superimposed substitutions. In 32 different pairwise comparisons between these mitochondrial and nuclear data sets, we used the maximum set of overlapping taxa. In each case, the variable-length bootstrap was used to resample at the size of the smaller data set. The nuclear exons consistently performed better than mitochondrial protein and rRNA-tRNA coding genes on a per-residue basis in recovering benchmark clades. We also concatenated nuclear genes for overlapping taxa and made comparisons with concatenated mitochondrial protein-coding genes from complete mitochondrial genomes. The variable-length bootstrap was used to score the recovery of benchmark clades as a function of the number of resampled base pairs. In every case, the nuclear concatenations were more efficient than the mitochondrial concatenations in recovering benchmark clades. Among genes included in our study, the nuclear genes were much less affected by superimposed substitutions. Nuclear genes having appropriate rates of substitution should receive strong consideration in efforts to reconstruct deep-level phylogenetic relationships. |
Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
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Higher-level mammalian phylogenetics remains an outstanding problem in systematics. Anatomical data suggest a moderately well resolved tree that includes several supraordinal groupings for the 18 orders of living placental mammals (Novacek 1992
; Shoshani and McKenna 1998
). Molecular sequence data have corroborated clades such as Cetartiodactyla (de Jong 1998
; Gatesy et al. 1999
; Liu and Miyamoto 1999
) and Paenungulata (Lavergne et al. 1996
; Springer et al. 1997a, 1997b
), challenged other morphological hypotheses (Graur, Hide, and Li 1991
; D'Erchia et al. 1996
; Arnason, Gullberg, and Janke 1997
; Janke, Xu, and Arnason 1997
; Springer et al. 1997a, 1997b
; Stanhope et al. 1998b
; Mouchaty et al. 2000
; Teeling et al. 2000
), and suggested new supraordinal associations (Graur and Higgins 1994
; Porter, Goodman, and Stanhope 1996
; Arnason, Gullberg, and Janke 1997
; Springer et al. 1997a, 1997b
; Stanhope et al. 1998b
; Liu and Miyamoto 1999
; Waddell, Okada, and Hasegawa 1999
; Mouchaty et al. 2000
). Recent attention in higher level mammalian and vertebrate molecular phylogenetics has focused on either protein-coding sequences from complete mitochondrial (mt) genomes (e.g., Krettek, Gullberg, and Arnason 1995
; D'Erchia et al. 1996
; Zardoya and Meyer 1997
; Rasmussen, Janke, and Arnason 1998
; Arnason, Gullberg, and Janke 1999
), mt rRNA gene sequences (Lavergne et al. 1996
; Springer et al. 1997a
; Stanhope et al. 1998a, 1998b
) or exonic regions of nuclear (nc) protein-coding genes (Porter, Goodman, and Stanhope 1996
; Madsen et al. 1997
; Stanhope et al. 1996, 1998a, 1998b
; Springer et al. 1997a, 1997b
; Gatesy et al. 1999
). A fundamental question that remains in this field is whether different types of mt or nc sequences are more reliable for recovering deep-level relationships such as those among orders of eutherian mammals (Springer et al. 1999
).
Molecular sequence data can be categorized in different ways, including by function (protein-coding vs. noncoding vs. structural RNA) and by genome (e.g., mitochondrial vs. nuclear). Different categories of sequences have distinct properties. In many groups, including mammals, the rate of nucleotide substitution among mt protein-coding genes is generally more rapid than the rate of nucleotide substitution among protein-coding regions of nc genes (Vawter and Brown 1986
). A second difference is that the mt genome is inherited as a single, haploid, nonrecombining linkage unit. This haploid mode of inheritance leads to a smaller effective population size compared with the nc genome. A smaller effective population size, in turn, results in a shorter expected coalescence time for mt loci compared with nc loci and a greater probability that the mt gene tree will accurately reflect the species tree for closely spaced internodes compared with nc gene trees (Moore 1995
). Arnason, Gullberg, and Janke (1999)
made specific reference to the problem of inferring the deep relationships among mammalian orders and suggested that mt data would be more efficient; i.e., nc data sets must be larger than mt data sets to achieve commensurate levels of resolution.
Several studies have compared the relative performances of individual mt genes in higher level phylogenetics using metrics such as the bootstrap support percentage and retention indices (Cao et al. 1994
; Cummings, Otto, and Wakeley 1995
; Zardoya and Meyer 1996
; Naylor and Brown 1997
). In this paper, we take an empirical approach to investigate the performance of several well-sampled mt and nc genes in recovering well-supported, deep-level mammalian clades. We find that the nc exons are more efficient and consistently achieve greater resolving power on a per-residue basis in comparison with equivalent lengths of either mt protein-coding genes or mt rRNA genes.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
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12S rRNA, tRNAVal, and 16S rRNA sequences were obtained for Dobsonia moluccensis (16S rRNA only; AF179290) and Tonatia bidens (AF179288) as described elsewhere (Springer, Hollar, and Burke 1995
; Springer et al. 1997b
). New interphotoreceptor retinoid binding protein (IRBP) exon 1 sequences were obtained for Erethizon dorsatum (AF179292), Tapirus pinchaque (AF179294), and Vulpes velox (AF179293) following Stanhope et al. (1992, 1996)
. Additional sequences for these and other genes were extracted from GenBank. The additional mt genes included cytochrome b, cytochrome oxidase subunit II (COII), and NADH dehydrogenase subunit I (ND1); these mt protein-coding genes were chosen because of their extensive taxonomic representation. Zardoya and Meyer (1996)
classified mt protein-coding genes into three groups (good, medium, and poor) based on their performance in recovering phylogenetically distant relatives. The mt protein-coding genes incorporated in our analysis included one gene (cytochrome b) in the good group and two genes (COII, ND1) in the medium group. Additional nc gene sequences included protein-coding regions of -2B adrenergic receptor (A2AB), aquaporin, ß-casein, -fibrinogen, -casein, protamine, and von Willebrand Factor (vWF). Among the nuclear genes, A2AB, IRBP, and vWF included representatives of all placental orders and marsupial outgroups. CLUSTAL W (Thompson, Higgins, and Gibson 1994
) was used to align 12S rRNA–tRNAVal–16S rRNA, COII, cytochrome b, ND1, A2AB, IRBP, and vWF sequences. Ambiguous regions of the 12S rRNA–tRNAVal–16S rRNA and COII alignments were excluded from the analyses. A short glutamic acid repeat region of the A2AB gene was also difficult to align and was omitted following Stanhope et al. (1998a)
. The aquaporin data set was from Madsen et al. (1997)
and Stanhope et al. (1998a)
, with additional sequences from GenBank (AJ277647, AJ251100, AJ251101). The ß-casein, -fibrinogen, -casein, and protamine data sets were from WHIPPO-2 (Gatesy et al. 1999
), with ambiguous regions of the alignment omitted following Gatesy et al. (1999)
. After removal of the ambiguous regions, the aligned data sets were the following lengths: 12S rRNA–tRNAVal–16S rRNA, 2,006 bp; cytochrome b, 1,152 bp; COII, 675 bp; ND1, 957 bp; A2AB, 1,164 bp; aquaporin, 333 bp; ß-casein, 520 bp; -fibrinogen, 679 bp, IRBP, 1,292 bp; -casein, 519 bp; protamine, 386 bp; and vWF, 1,251 bp. Alignments, as well as accession numbers for all sequences, are available on request from mark.springer@ucr.edu.
Phylogenetic analyses were performed for 32 different pairwise comparisons between an mt data set and an nc data set. In each case, we used the maximum set of overlapping eutherian and metatherian taxa (appendix); some taxa were chimeric (appendix). For example, Elephas and Loxodonta are both in the order Proboscidea, and it was necessary to use a nuclear sequence for Elephas and a mitochondrial sequence for Loxodonta in some comparisons. For all pairwise comparisons, the variable-length bootstrap was used to resample at the size of the smaller data set. For example, in the comparison between A2AB and COII, we resampled both data sets at the size of COII because it was the smaller (675 bp) of the two data sets. Use of the variable-length bootstrap permitted us to assess performance on a per-residue basis. We evaluated the performance of the mt and the nc data sets, respectively, in recovering deep-level, benchmark clades where monophyly is generally agreed upon and where available sequences index intraclade divergences that are no later than the Eocene based on the current fossil record (McKenna and Bell 1997
). One exception is the Australasian marsupial order Diprotodontia, for which intraclade divergences based on first fossil occurrences are Oligocene (Woodburne et al. 1993
; Woodburne and Case 1996
). However, most workers accept an earlier age based on the incompleteness of the Paleogene Australian fossil record coupled with molecular-clock estimates (Springer and Kirsch 1991
; Woodburne and Case 1996
; Kirsch, Lapointe, and Springer 1997
); the latter consistently place the split between vombatiform and phalangeriform diprodotontians in the late Paleocene or Eocene (Springer and Kirsch 1991
; Kirsch, Lapointe, and Springer 1997
). Benchmark clades that were evaluated were as follows: Carnivora (canoids + feloids), Cetacea (mysticetes + odontocetes), Cetartiodactyla (artiodactyls + cetaceans), Chiroptera (megachiropterans + microchiropterans), Diprotodontia (phalangeriforms + vombatiforms), Eutheria (a minimum of 13 of 18 placental orders were represented in tests to recover Eutheria), Paenungulata (hyracoids + proboscideans + sirenians), Perissodactyla (ceratomorphs + hippomorphs), Primates (strepsirhines + haplorhines), Ruminantia (tragulines + pecorans), Suina (suids + tayassuids), and Xenarthra (infraorder Pilosa + infraorder Cingulata; sensu Nowak and Paradiso 1983
). Chiropteran monophyly and the paenungulate hypothesis have previously been questioned (e.g., Pettigrew [1986
] challenged bat monophyly, and Prothero and Schoch [1989
] argued against the Paenungulata), but recent work provides compelling support in favor of these clades (Wible and Novacek 1988
; Stanhope et al. 1992, 1996, 1998a, 1998b
; Simmons 1994
; Kirsch et al. 1995
; Lavergne et al. 1996
; Porter, Goodman, and Stanhope 1996
; Springer et al. 1997b, 1999
). Afrotheria, Eulipotyphla, hippo + Cetacea, and Rodentia were not scored as benchmark clades because of controversy surrounding these hypotheses. Afrotheria is supported by molecular data (Stanhope et al. 1998b
), but not by morphological data (Asher 1999); Eulipotyphla (Erinaceidae + Soricidae + Talpidae + Solenodontidae; Waddell, Okada, and Hasegawa 1999
) is supported by nuclear genes (Stanhope et al. 1998b
), but not by mt genome data (Mouchaty et al. 2000
); hippo + Cetacea is supported by molecular data, but not by morphological data (O'Leary and Geisler 1999
); and rodent monophyly remains controversial (Graur, Hide, and Li 1991
; D'Erchia et al. 1996
; Reyes, Pesole, and Saccone 1998
; Penny et al. 1999
).
In addition to pairwise comparisons between individual mt and nc data sets, we compared concatenated nc genes with concatenated mt protein-coding genes from mt genomes. First, concatenated sequences for the three nc genes with the most extensive taxonomic representation (A2AB, IRBP, vWF; total length = 3,707 bp) were compared with mt protein-coding genes (total length = 9,828 bp); this comparison included 20 overlapping taxa and permitted scoring of support for four benchmark clades (Carnivora, Cetartiodactyla, Eutheria, and Perissodactyla). Overlapping taxa were as follows: Bos, Canoidea (Canis, Phoca, or Vulpes), Ceratomorpha (Ceratotherium, Diceros, or Tapirus), Didelphis, Diprotodontia (Macropus or Vombatus), Equus, Erinaceus, Felis, Hippopotamus, Homo, Hystricognathi (Cavia, Dasyprocta, or Erethizon), Muridae (Mus or Rattus), Mysticeti (Balaenoptera or Megaptera), Orycteropus, Oryctolagus, Phyllostomidae (Artibeus, Macrotus, or Tonatia), Proboscidea (Elephas or Loxodonta), Soricomorpha (Sorex, Scalopus, or Talpa), Sus, and Xenarthra (Bradypus or Dasypus). We also examined support for the controversial hypotheses Afrotheria and hippo + Cetacea. Second, we added ß-casein, -fibrinogen, and -casein to the nuclear concatenation (total length = 5,425 bp). This resulted in 11 overlapping taxa between the mt and nc concatenations as follows: Bos, Canoidea (Canis, Phoca, or Vulpes), Ceratomorpha (Ceratotherium, Dicerorhinus, Diceros, or Tapirus), Equus, Felis, Hippopotamidae (Hexaprotodon or Hippopotamus), Homo, Muridae (Mus or Rattus), Mysticeti (Balaenoptera or Megaptera), Orycteropus, and Sus. With these 11 taxa, it was possible to score support for the benchmark clades Carnivora, Cetartiodactyla, and Perissodactyla, as well as the more controversial hippo + Cetacea hypothesis. To obtain a concatenation of mt protein-coding sequences, we used the Mouchaty et al. (2000)
mt data set and added Loxodonta (African elephant; AJ224821). Ambiguous and gapped regions were not included in the analyses following Mouchaty et al. (2000)
.
Phylogenetic analyses included unweighted and weighted parsimony and minimum evolution with logdet (Lockhart et al. 1994
) and maximum-likelihood distances, the latter under both the HKY85 (Hasegawa, Kishino, and Yano 1985
) and the GTR models of sequence evolution with maximum-likelihood estimates of the substitution parameterizations. The HKY85 model was also employed with additional allowances for a gamma distribution (
) of rates and a fraction of invariant sites (I); both of these parameters were estimated with maximum likelihood from minimum-length parsimony trees. Third codon positions of mt protein-coding genes are known to be saturated, or nearly so, at deep phylogenetic levels (see below). We therefore examined the effect of downweighting third positions by either assigning zero weight or employing transversion parsimony. We also employed amino acid parsimony with the mt protein-coding genes. In all analyses, branches were swapped using the tree bisection-reconnection branch-swapping option. Parsimony analyses employed 10 random input orders per replicate, with gaps treated as missing data. All phylogenetic analyses were performed with PAUP, versions 4.0b2 and 4.0b3 (Swofford 1998
).
For data sets that included marsupial outgroups, we compared the percentages of sequence divergence for three intraordinal/interordinal splits within Eutheria, all of which are in the range of 50–60 Myr based on the fossil record and molecular data (Bos to Cetacea [Balaenoptera]; Felis to Canis; Hyracoidea [Procavia] to Sirenia [Dugong]) (Garland et al. 1993
; Arnason and Gullberg 1996
; Springer 1997
), with the divergence between these same placentals and a marsupial (Didelphis). The timing of the latter split is 97–160 Myr based on different types of data, with most estimates in the range of 100–130 Myr (Rowe 1993
; Springer 1997
; Kumar and Hedges 1998
), approximately double that for the three intraplacental splits. 
values were calculated as the increase in sequence divergence (uncorrected) in the placental-marsupial comparison relative to the mean value for the three intraplacental comparisons. values index the amount of sequence divergence that is available for resolving relationships that are deeper than the three intraplacental splits but shallower than the marsupial-placental split. values were calculated with uncorrected distances to highlight the effects of superimposed substitutions. Corrected distances, by definition, are employed to eliminate the effects of superimposed substitutions.
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
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Figure 1 and table 1 show the results of comparisons between nc and mt genes with different methods of phylogenetic analysis. Figure 1 plots bootstrap support values for nc versus mt genes for all of the phylogenetic methods that we employed. Nine of nine panels show comparisons between nc genes and mt protein-coding genes (filled squares); five of nine panels also show comparisons between nc genes and mt RNA genes (open squares). Data points that fall on the diagonal lines correspond to cases where nc and mt bootstrap support percentages are equivalent. Data points above the diagonal lines show cases where mt support exceeds nc support. Data points below the diagonal lines show cases where nc support exceeds mt support. Table 1 summarizes the numbers of cases for which nc bootstrap support was higher for a benchmark clade, the numbers of cases for which bootstrap support was equal, and the numbers of cases for which mt bootstrap support exceeded nc support. Table 1 also shows mean bootstrap support (for all benchmark clades) for both nc and mt genes with different phylogenetic methods.
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For comparisons between mt protein-coding genes and nc genes, there were 106 benchmark clades that were scored across 24 pairwise comparisons between individual nc and mt data sets. Support deriving from the nc genes exceeded support deriving from the mt protein-coding genes in 90–100 of the 106 cases with different phylogenetic methods (fig. 1 and table 1 ). A dense concentration of data points (filled squares) below the diagonal lines is evident in all of the panels in figure 1 and illustrates the superior performance of the nc genes. Mean bootstrap support was always higher for the nc genes (table 1 ). Whereas mean mt support ranged from 30.7% (parsimony with zero weight at third codon positions) to 43.8% (minimum evolution–
+I), nc support ranged from 84.3% (minimum evolution–+I) to 89.6% (minimum evolution–HKY85). The difference in mean bootstrap ranged from 40.5% (minimum evolution–+I vs. minimum evolution–+I) to 56.0% (parsimony vs. parsimony with zero weight at third codon positions). Mitochondrial RNA genes performed better than mt protein-coding genes in comparisons against the nc genes. Benchmark clades were scored across eight pairwise comparisons between individual nc and mt RNA data sets. Bootstrap support scores were higher for nc genes in 31–33 of the 42 cases (fig. 1 and table 1 ). Mean support scores for nc genes were higher than those for mt RNA genes with all phylogenetic methods. Nevertheless, differences between means were always less than those for comparisons between nc genes and mt protein-coding genes. Differences in mean support ranged from 16.5% to 24.3% (table 1 ).
In all comparisons between the 3 or 6 concatenated nc genes and the 12 concatenated mt protein-coding genes from complete mt genomes, both nc and mt genes showed increased support for all of the benchmark clades as a function of the number of resampled nucleotides. However, the nc genes were always more efficient than the mt genes in recovering benchmark clades (figs. 2 and 3 ). This was especially noticeable for Cetartiodactyla, with both parsimony (figs. 2A and 3A ) and minimum evolution (figs. 2B and 3B ). The more controversial clades (Afrotheria; Hippopotamidae + Cetacea) were also recovered with greater efficiency with the nc data (figs. 2 and 3 ).
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Among the data sets that included marsupial outgroups,
values for all substitutions were highest for the three nc genes. Furthermore, these values exceeded sequence divergence values for the intraplacental comparisons for all three nc genes (table 2
). Among the mt protein-coding genes, values (all substitutions) were always less than the intraplacental divergences (table 2
).
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Among nc genes, transitions and transversions showed positive
values both at first + second and at third positions. For transversions, values both at first + second and at third positions were higher than intraplacental divergences. For transitions, values at first + second positions were always higher than intraplacental divergences; at third positions, transition values were higher than intraplacental divergences for A2AB but lower than intraplacental divergences for IRBP and vWF.
Among mt protein-coding genes, transversion values were higher than intraplacental divergences at first + second positions but lower than intraplacental divergences at third positions. Transition values at first + second positions were lower than intraplacental divergence values except in one instance—the caniform-to-feliform divergence for COII. Third-position transitions of mt protein-coding genes were saturated (mean value = -0.83; table 2
).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
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Our results suggest that mt genes have less resolving power than certain nc exons in recovering deep-level mammalian clades. This result was obtained for comparisons between individual mt and nc genes, as well as for comparisons between concatenated nc genes and concatenated mt protein-coding genes from mt genomes. Given that the nc genes exhibited the highest absolute
values and that values exceeded intraplacental divergences, it is not surprising that they performed better than mt genes in recovering deep-level clades. We would not expect all types of nc sequences to perform as well as the sequences that were included in our study. Clearly, the exonic sequences included in our study constitute a biased sample from the nc genome. Nevertheless, there is almost unlimited potential for choosing exonic regions with appropriate rates of sequence evolution that allow for the recovery of deep-level mammalian clades. Even though the nc exons performed better than mt genes in recovering deep-level clades, phylogenetic analyses based on mt sequences remain valuable. Complete mt genomes contain considerably more resolving power than single mt genes and have provided strong support for some of the same deep-level clades that are supported by nc sequences, e.g., Hippopotamidae + Cetacea (Ursing and Arnason 1998
; Gatesy et al. 1999
). Indeed, our comparisons were based on the variable-length bootstrap, which was employed for purposes of evaluating mt and nc sequences on a per-residue basis. Even in our comparisons between concatenated sequences from the mt and nc genomes, the variable-length bootstrap allowed for resampling only at a maximum size of 5,424 bp (fig. 3
). Given that mt protein-coding sequences from complete genomes are approximately twice this length and that mt protein-coding sequences are sometimes analyzed in conjunction with mt rRNA sequences, mt genomes provide more resolving power than is evident from figs. 2 and 3
(e.g., see Reyes et al. 2000
). The value of mt sequences in phylogenetic analyses is further enhanced if they are collected in conjunction with nc sequences, because they provide an independent estimate of phylogenetic relationships that can be compared with estimates based on nc sequences.
The hypothesis of Arnason, Gullberg, and Janke (1999)
that nc alignments must be longer than mt alignments to achieve equivalent levels of resolution is strongly contradicted for the nc exons that we examined. Rather, nc exons recovered benchmark clades with higher efficiency. This result suggests that internodal divergence times for the clades considered in this study are not excessively short compared with coalescence times for nc genes. Nuclear genes included in our study represent several unlinked loci, yet each gene individually supports the same widely accepted clades. The conclusion that these nc genes are superior to mt genes in recovering expected relationships does not appear to be the result of selecting poorly performing mt genes. Zardoya and Meyer (1996)
classified mt protein-coding genes into three groups (good, medium, and poor) based on their performance in recovering phylogenetically distant relatives. The mt protein-coding genes incorporated in our analysis included one gene (cytochrome b) in the good group and two genes (COII, ND1) in the medium group. Furthermore, our comparisons between concatenated mt and nc genes included 12 of 13 protein-coding genes from the mt genome (ND6 was excluded because it is coded on the light strand and has properties different from those of the other 12 protein-coding genes; Waddell et al. 1999
).
One factor that may contribute to the differences in performance among the sequences we examined is the rate of nucleotide substitution. Based on the intraplacental divergences reported in table 2
, overall rates of nucleotide substitution are highest among the mt protein-coding genes, followed by vWF, IRBP, rRNA, and A2AB. A consequence of the higher substitution rates among the mt protein-coding genes is saturation over shorter lookback times. Less among-sites rate variation among the nc genes may also contribute to differences in performance between the nc and the mt genes. For the 32 pairwise comparisons we performed, maximum-likelihood estimates of the shape parameter () for the gamma distribution were estimated with and without an allowance for invariant sites (I). Without an allowance for I, was higher for the nc gene than for the mt gene in every comparison. With an allowance for I, was higher for the nc gene in 31 of 32 comparisons ( for mt RNA was higher than for aquaporin in the mt RNA–aquaporin comparison). With or without I, it appears that substitutions are more evenly distributed among the nc genes and there is less of a tendency for substitutions to occur repeatedly at the same sites.
Mitochondrial protein-coding genes have until now attracted most attention in studies of higher-level relationships for some groups, e.g., classes of vertebrates. Our results suggest that select nc genes may be more appropriate for reconstructing phylogenetic relationships among higher-level taxa. The use of nc sequences to examine phylogenetic relationships is especially important in cases where mt protein-coding genes have suggested hypotheses that do not accord with traditional views (Curole and Kocher 1999
).
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
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This work was supported by grants from the National Science Foundation (DEB-9419617 and DEB-9903810 to M.S.S.) and the Nuffield Foundation and the Royal Society (to M.J.S.) and a European Commission–TMR grant (ERB-FMRX-CT98-0221) to M.J.S. and W.W.d.J. We thank two anonymous referees for helpful comments on an earlier version of this manuscript. Dr. Ulfur Arnason kindly supplied mt alignments.
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Footnotes |
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Dan Graur, Reviewing Editor
1 Keywords: Mammalia
mitochondrial DNA
nuclear DNA
phylogeny reconstruction 
2 Address for correspondence and reprints: Mark Springer, Department of Biology, University of California, Riverside, California 92521. E-mail: mark.springer{at}ucr.edu
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsliterature cited |
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