*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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Introduction |
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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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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 5060 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 97160 Myr based on different types of data, with most estimates in the range of 100130 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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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 3133 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 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 instancethe 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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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 RNAaquaporin 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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Footnotes |
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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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