Department of Genetics, Division of Evolutionary Molecular Systematics, University of Lund, Lund, Sweden
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Based on detailed morphological analysis, Butler (1988)
concluded that monophyly of Lipotyphla was supported by six shared derived characters (synapomorphies), but only two of these characters (hindgut simplification, reduction of the pubic symphysis) were considered synapomorphic by MacPhee and Novacek (1993)
. Although relationships among lipotyphlan families have been uncertain because of the morphological diversity of the group (Butler 1972
), morphological and paleontological evidence is commonly interpreted as supporting two relationships: (1) ancient origin and clear morphological distinction of the Erinaceidae and (2) a close relationship between Talpidae and Soricidae (Butler 1988;
Carroll 1988
; MacPhee and Novacek 1993
).
The relationship of the Lipotyphla to the other orders of eutherian mammals has remained a major problem in mammalian phylogeny (Butler 1972
; Novacek 1992
). The combination of numerous plesiomorphic "primitive" traits and specialized adaptations of the lipotyphlans has confounded attempts to conclusively determine the phylogenetic position of Lipotyphla by morphological comparison, and recent cladistic analyses of morphological data have left Lipotyphla in an unresolved polytomy near the base of the eutherian tree (Novacek, Wyss, and McKenna 1988
; Novacek 1992
). Phylogenetic analyses of large mitochondrial data sets support an early divergence of the hedgehog lineage (Erinaceidae) from the rest of Eutheria (Krettek, Gullberg, and Arnason 1995
; DErchia et al. 1996
; Janke, Xu, and Arnason 1997
; Penny and Hasegawa 1997
). However, resolution of the phylogenetic position of Lipotyphla as a whole in these analyses, with the hedgehog as its only representative, depends on the monophyly of Lipotyphla as a taxonomic unit.
Although recent morphological reviews (Butler 1988;
MacPhee and Novacek 1993
) concur on the composition of Lipotyphla, recent molecular studies (Lavergne et al. 1996
; Springer et al. 1997
; Stanhope et al. 1998
) have indicated that Lipotyphla are polyphyletic, with the tenrecs and golden moles being members of a clade composed mainly of taxa endemic to the African continent, to the exclusion of the non-African lipotyphlan families. An important difference between the results of Stanhope et al. (1998)
, which were based on nuclear genes and combined trees, and results based on large mitochondrial data sets (Krettek, Gullberg, and Arnason 1995
; DErchia et al. 1996
; Arnason, Gullberg, and Janke 1997
; Janke, Xu, and Arnason 1997
) is the position of this non-African lipotyphlan clade. Stanhope et al. (1988)
found that the mole and the hedgehog formed the sister group to Artiodactyla (represented by the cow), while the mitochondrial analyses have consistently placed the hedgehog as the outgroup to all other eutherians.
In this study, we determined the sequence of the complete mtDNA genome of the mole Talpa europaea (family Talpidae) and reconstructed the phylogenetic relationship of the mole to the hedgehog and 22 other eutherian taxa. We also sequenced the complete mitochondrial cytochrome b gene of the shrew Sorex araneus (Soricidae) in order to establish the affinities between the families Talpidae and Soricidae.
![]() |
Materials and Methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The mole was analyzed along with the following species: the platypus Ornithorhynchus anatinus (Janke et al. 1996
); the opossum Didelphis virginiana (Janke et al. 1994
); the wallaroo Macropus robustus (Janke, Xu, and Arnason 1997
); the hedgehog Erinaceus europaeus (Krettek, Gullberg, and Arnason 1995
); the mouse Mus musculus (Bibb et al. 1981
); the rat Rattus norvegicus (Gadaleta et al. 1989
); the guinea pig Cavia porcellus (DErchia et al. 1996
); the rabbit Oryctolagus cuniculus (Gissi, Gullberg, and Arnason 1998
); the gibbon Hylobates lar (Arnason, Gullberg, and Xu 1996
); the human, Homo sapiens (Arnason, Xu, and Gullberg 1996
); the aardvark Orycteropus afer (Arnason, Gullberg, and Janke 1999
); the armadillo Dasypus novemcinctus (Arnason, Gullberg, and Janke 1997
); the fruit bat Artibeus jamaicensis (Pumo et al. 1998
); the harbor seal Phoca vitulina (Arnason and Johnsson 1992
); the dog Canis familiaris (Kim et al. 1998
); the domestic cat Felis catus (Lopez et al. 1996
); the horse Equus caballus (Xu and Arnason 1994
); the donkey E. asinus (Xu, Gullberg, and Arnason 1996
); the Indian rhinoceros Rhinoceros unicornis (Xu, Janke, and Arnason 1996
) the white rhinoceros Ceratotherium simum (Xu and Arnason 1997
); the pig Sus scrofa (Ursing and Arnason 1998a
); the cow Bos taurus (Anderson et al. 1982
); the sheep Ovis aries (Hiendleder et al. 1998
); the hippopotamus, Hippopotamus amphibius (Ursing and Arnason 1998b
); the fin whale, Balaenoptera physalus (Arnason, Gullberg, and Widegren 1991
); and the blue whale, Balaenoptera musculus (Arnason and Gullberg 1993
).
The phylogenetic analyses were based on the concatenated sequences of 12 mitochondrial protein-coding genes, excluding the L-strand-encoded NADH6 gene, the composition of which deviates from that of the H-strand-encoded genes. After removing gaps and ambiguous sites adjacent to gaps, the resulting alignment contained 9,870 nt, corresponding to 3,290 amino acids (aa). The analyses were based on both amino acid and nucleotide sequences of first plus second codon positions, with the first positions of leucine codons coded as Y (pyrimidine). Three different methods of phylogenetic reconstruction were used: maximum parsimony (MP; Fitch 1971
), neighbor joining (NJ; Saitou and Nei 1987
), and maximum likelihood (ML; Felsenstein 1981
). The PUZZLE, version 4.01 (Strimmer and von Haeseler 1996
), and MOLPHY (Adachi and Hasegawa 1996a)
programs were used for ML analyses, in which we applied the mtREV-24 rate matrix (Adachi and Hasegawa 1996b
) and the HKY model of sequence evolution (Hasegawa, Kishino, and Yano 1985
). The same models were used to generate distance matrices for NJ analysis. The ML analysis was performed assuming rate homogeneity and rate heterogeneity with four categories of variable sites and one category of invariable sites. The MP and NJ analyses were carried out using the PHYLIP package (Felsenstein 1991
). The support for different positions of the mole and the hedgehog within the eutherian tree was investigated both separately and in combination by comparing the log likelihood values obtained from ML analyses of the various topologies.
Phylogenetic analyses of the cytochrome b gene included S. araneus, along with the taxa included in the study of complete mtDNAs. The length of the cytochrome b alignment was 1,122 nt, corresponding to 374 aa, after removal of 18 nt (6 aa) of ambiguous homology at the 3' end of the gene. The cytochrome b data were analyzed in the same way as the large mitochondrial alignment. Partial sequences of the cytochrome b genes of a number of soricids have been reported by Ohdachi et al. (1997)
and Fumagalli et al. (1999)
. Analyses of these sequences placed the soricids on a common branch as the sister group of the mole (data not shown).
Congruence with previously published phylogenetic hypotheses based on nuclear data sets, exon 28 of the von Willebrand factor gene (vWF, 318 aa), and the alpha-2 B-adrenergic receptor gene (A2AB, 378 aa), reported by Stanhope et al. (1998)
, was tested with the nonparametric test suggested by Templeton (1983)
. The test included the seven taxa represented by both vWF and A2AB: the hedgehog, the rat, the rabbit, the human, the mole, the horse, and the cow. The best tree topology for each data set was determined by MP, NJ, and ML. The analyses were performed on all codon positions, as well as on first plus second codon positions. The support of the nuclear sequences for the best mitochondrial tree was also tested.
![]() |
ResultsCharacteristics of the mtDNA of Talpa europaea |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Phylogenetic Analysis and the Divergence Between Talpa, Chiroptera, and the Cetferungulates
Consistent with a previous study (Krettek, Gullberg, and Arnason 1995
), the hedgehog represented the most basal eutherian taxon; however, the mole was not found to be the sister group of the hedgehog, as would be expected if Lipotyphla were monophyletic. Instead, the mole was identified as the sister group of the Chiroptera. The position of the Talpa/Chiroptera clade was immediately basal to the cetferungulates (fig. 1
). This phylogenetic relationship was strongly supported by all three analytical approaches used (MP, NJ, and ML) and was not affected by exclusion of the hedgehog. table 1
summarizes the bootstrap and quartet puzzle (QP) support values for the branches relevant to the positions of the mole and the hedgehog in the eutherian tree.
|
|
|
ML distances calculated using the mtREV-24 model of amino acid sequence evolution (Adachi and Hasegawa 1996b
) were used to estimate the divergence times between the mole and the bat, as well as the origin of the mole/bat clade. The molecular clock was calibrated with the two references A/C-60, the divergence between ruminant Artiodactyla and Cetacea 60 MYA (Arnason and Gullberg 1996
), and E/R-50, the divergence between Equidae and Rhinocerotidae 50 MYA (Xu, Janke, and Arnason 1996
; Arnason, Gullberg, and Janke 1998
). Both references yielded consistent datings, according to which the mole and the bat lineages split
74 MYA, while the corresponding dating for the divergence between the mole/bat clade and the cetferungulates was
79 MYA. In a previous study, the cetferungulate origin was defined as occurring at the divergence of edentates and cetferungulates (Arnason, Gullberg, and Janke 1997
). The present study further constrains the cetferungulate origin by placing it at the divergence between Talpa/Chiroptera and the cetferungulate clade.
The branches defining the positions of the guinea pig and the rabbit have been collapsed in figure 1
, as they were not consistently identified by all data sets and analyses. The limited resolution in these parts of the tree have been discussed previously (Arnason, Gullberg, and Janke 1997, 1999
; Janke, Xu, and Arnason 1997
) and therefore are not detailed here. The other relationships shown in figure 1
have been described and dated in previous studies (Janke et al. 1994
; Xu, Janke, and Arnason 1996
; Janke, Xu, and Arnason 1997
).
ML analysis of nucleotide sequences using the HKY model of sequence evolution and rate heterogeneity with eight classes of variable sites or four classes of variable sites plus one class of invariable sites did not resolve the phylogenetic position of the hedgehog relative to other eutherian orders, as the lnL differences for the various positions of this taxon differed only marginally. It is probable that this poor resolution is related to the significantly deviating nucleotide composition of the hedgehog. The same analysis using amino acid sequences, however, confirmed a basal position of the hedgehog (table 2 ).
Comparison of Different Data Sets
In contrast to the findings presented here, which are based on an alignment with a length of almost 10,000 nt, analyses of nuclear sequences (exon 28 of the vWF gene and the A2AB gene) and of combined nuclear and mitochondrial ribosomal (12S and 16S rDNA) sequences support a mole + hedgehog clade well within the eutherian tree (Stanhope et al. 1998
). To investigate possible reasons for this inconsistency, we examined the relative phylogenetic signals in the sequences reported by Stanhope et al. (1998)
. This examination (table 3
) revealed significant (2
) inconsistencies between the phylogenetic signals of the two nuclear sequences and between the vWF and the mitochondrial rDNA data sets, indicating that these genes are subject to differing evolutionary processes or constraints (Bull et al. 1993
; de Queiroz, Donoghue, and Kim 1995
).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A nonbasal position of the hedgehog was shown in a tree reported by Sullivan and Swofford (1997)
. The findings which were based on a rate heterogeneity model and ML analysis of mitochondrial nucleotide sequences were inconclusive, however, as to the definite position of the hedgehog. The study included no amino acid analysis, and the possible influence of the significantly biased base composition of the hedgehog relative to the other eutherians was not discussed. When rate heterogeneity is taken into account in the ML analysis of amino acid sequences, as in the present study, the hedgehog remains the most basal eutherian taxon. Under the same model of sequence evolution, the monophyly of the mole (Talpidae) and the hedgehog (Erinaceidae) could be excluded with high statistical support. The amino acid composition of the hedgehog does not differ significantly from that of other taxa, even though it remains the most deviating; all analyses of this data set placed the hedgehog basal among the eutherians.
Analyses of two nuclear (vWF and A2AB) and mitochondrial rDNA sequences have supported a sister group relationship between the hedgehog and the mole (Stanhope et al. 1998
), but trees reconstructed from the analyses showed some inconsistencies, and several ordinal relationships which have received conclusive support in studies of complete mitochondrial genomes remained unresolved. Thus, the analyses of Stanhope et al. (1998)
disrupted some phylogenetic relationships, such as the cetferungulate clade, which have been strongly supported in analyses of complete mtDNAs (Arnason et al. 1996
; DErchia et al. 1996
; Xu, Janke, and Arnason 1996
; Arnason, Gullberg, and Janke 1997, 1998
; Janke, Xu, and Arnason 1997
; Ursing and Arnason 1998a, 1998b
). Our examination of the vWF and A2AB data sets showed that they favored different phylogenies, with the vWF data set containing a strong signal for the mole + hedgehog clade. However, at the same time, vWF did not support other relationships, such as the affinity between Artiodactyla and Perissodactyla, which have been identified in other molecular studies. Our examination of these findings (see table 3
) indicate that the vWF and A2AB genes are under different evolutionary constraints, which may result in gene phylogenies deviating from the evolutionary history of the species harboring these sequences. Comparable studies of mitochondrial protein-coding genes (Cao et al. 1994, 1998
) have shown that among the H-strand- encoded genes, only one, NADH1, provides a phylogeny which with respect to one taxon, the rodents, deviates markedly from reconstructions based on the concatenated sequences of all mitochondrial protein-coding genes. Even so, the deviation in this case was still less pronounced than that occurring in the nuclear data sets used by Stanhope et al. (1998)
.
The phylogenetic position of Lipotyphla has remained obscure in morphological studies because of the combination of numerous "primitive" traits and specialized adaptations of lipotyphlan families. Cladistic analyses of morphological characters have recognized Lipotyphla as both monophyletic and basal in the eutherian tree (Novacek and Wyss 1986
; Novacek, Wyss, and McKenna 1988
; Novacek 1989, 1990
). The present molecular analyses of 12 mitochondrial protein-coding genes do not support lipotyphlan monophyly. Instead, a phylogenetic position of the hedgehog at a basal position in the eutherian tree and of the mole/bat as the sister group of the cetferungulates was strongly supported by all three methods of phylogeny reconstruction used, MP, NJ, and ML (table 1
). Alternative placements of the mole were without statistical support (table 2
). Inclusion or exclusion of the hedgehog did not affect the position of the mole. The results challenge the retention of the Lipotyphla as a monophyletic systematic unit. Furthermore, the findings support phylogenetic reevaluation of several morphological characteristics, as proposed in a recent provocative study of eutherian evolution (Werdelin and Nilsonne 1999
).
Morphologists have long recognized a clear distinction between moles and hedgehogs, advocating separation of the Lipotyphla into two primary lineages, the Erinaceomorpha, with the family Erinaceidae, and the Soricomorpha, traditionally including the shrews (Soricidae) and the talpid moles (Gregory 1910
; Butler 1972, 1988
; McKenna 1975
). As discussed by MacPhee and Novacek (1993)
the morphological evidence in support of lipotyphlan monophyly is weak, and the molecular results indicating lipotyphlan polyphyly are therefore not contradicted by morphological conclusions. The most important result of the present study is the strong statistical support for the phylogenetic position of Talpidae distant from the Erinaceidae in the eutherian tree. Furthermore, our results support the traditional view of a close phylogenetic relationship between Soricidae and Talpidae in the Soricoidea (Gregory 1910
; Hutchinson 1968
; Butler 1972, 1988
). McDowell (1958)
and McKenna and Bell (1997)
have suggested a sister group relationship between Talpidae and Erinaceidae. The morphological support for this relationship is not strong, however, and the characters listed by McDowell have been interpreted as being plesiomorphic (Butler 1988
).
The molecular data presented here are consistent with the placement of the families Talpidae and Soricidae within the Soricomorpha (Gregory 1910
; McKenna 1975
; Butler 1972, 1988
; MacPhee and Novacek 1993
) and the ordinal-level classification of the Erinaceomorpha and Soricomorpha (McKenna 1975
). The study has placed the Erinaceomorpha and the Soricomorpha at very different positions in the eutherian phylogenetic tree, a finding that is inconsistent with lipotyphlan monophyly.
![]() |
Acknowledgements |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Footnotes |
---|
1 Keywords: Phylogenetics,
insectivore,
Lipotyphla,
mole,
Talpa europaea,
mitochondrial DNA.
2 Address for correspondence and reprints: Ulfur Arnason, Department of Genetics, Division of Evolutionary Molecular Systematics, University of Lund, Sölvegatan 29, S-223 62 Lund, Sweden. E-mail: ulfur.arnason{at}gen.lu.se
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Adachi, J., and M. Hasegawa. 1996a. MOLPHY version 2.3: programs for molecular phylogenetics based on maximum likelihood. Comput. Sci. Monogr. 28:1150.
. 1996b. Model of amino acid substitution in proteins encoded by mitochondrial DNA. J. Mol. Evol. 42:459468.
Anderson, S., M. H. L. de Bruijn, A. R. Coulson, I. C. Eperon, F. Sanger, and I. G. Young. 1982. Complete sequence of bovine mitochondrial DNA. J. Mol. Biol. 156:683717.[ISI][Medline]
Arnason, U., and A. Gullberg. 1993. Comparison between the complete mtDNA sequences of the blue and the fin whale, two species that can hybridize in nature. J. Mol. Evol. 37:312322.[ISI][Medline]
. 1996. Cytochrome b nucleotide sequences and the identification of five primary lineages of extant cetaceans. Mol. Biol. Evol. 13:407417.[Abstract]
Arnason, U., A. Gullberg, and A. Janke. 1997. Phylogenetic analyses of mitochondrial DNA suggest a sister group relationship between Xenarthra (Edentata) and ferungulates. Mol. Biol. Evol. 14:762768.[Abstract]
. 1998. Molecular timing of primate divergences as estimated by two non-primate calibration points. J. Mol. Evol. 47:718727.[ISI][Medline]
. 1999. The mitochondrial DNA molecular of the aardvark, Orycteropus afer, and the position of the Tubulidentata in the eutherian tree. Proc. R. Soc. Lond. B Biol. Sci. 22:339345.
Arnason, U., A. Gullberg, A. Janke, and X. Xu. 1996. Pattern and timing of evolutionary divergences among hominoids based on analyses of complete mtDNAs. J. Mol. Evol. 43:650661.[ISI][Medline]
Arnason, U., A. Gullberg, and B. Widegren. 1991. The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balaenoptera physalus. J. Mol. Evol. 33:556568.[ISI][Medline]
Arnason, U., A. Gullberg, and X. Xu. 1996. A complete mitochondrial DNA molecule of the white-handed gibbon, Hylobates lar, and comparison among individual mitochondrial genes of all hominoid genera. Hereditas 124:185189.
Arnason, U., and E. Johnsson. 1992. The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J. Mol. Evol. 34:493505.[ISI][Medline]
Arnason, U., X. Xu, and A. Gullberg. 1996. Comparison between the complete mitochondrial sequences of Homo and the common chimpanzee based on non-chimaeric sequences. J. Mol. Evol. 41:952957.[ISI]
Bibb, M. J., R. A. Van Etten, C. T. Wright, M. W. Walberg, and D. A. Clayton. 1981. Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167180.
Bull, J. J., J. P. Huelsenbeck, C. W. Cunningham, D. L. Swofford, and P. J. Waddell. 1993. Partitioning and combining data in phylogenetic analyses. Syst. Biol. 42:384397.[ISI]
Butler, P. M. 1972. The problem of insectivore classification. Pp. 253265 in K. A. Joysey and T. S. Kemp, eds. Studies in vertebrate evolution. Winchester Press, New York.
. 1988. Phylogeny of the insectivores. Pp. 117141 in M. J. Benton, ed. The phylogeny and classification of the tetrapods, Vol. 2. Mammals. Clarendon Press, Oxford, England.
Cao, Y., J. Adachi, A. Janke, S. Pääbo, and M. Hasegawa. 1994. Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene. J. Mol. Evol. 39:519527.[ISI][Medline]
Cao, Y., A. Janke, P. J. Waddell, M. Westerman, O. Takenaka, S. Murata, N. Okada, S. Paabo, and M. Hasegawa. 1998. Conflict amongst individual mitochondrial proteins in resolving the phylogeny of eutherian orders. J. Mol. Evol. 47:307322.[ISI][Medline]
Carroll, R. L. 1988. Vertebrate paleontology and evolution. Freeman, New York.
DErchia, A. M., C. Gissi, G. Pesole, C. Saccone, and U. Arnason. 1996. The guinea-pig is not a rodent. Nature 381:597599.
de Queiroz, A., M. J. Donoghue, and J. Kim. 1995. Separate versus combined analysis of phylogenetic evidence. Annu. Rev. Ecol. Syst. 26:657681.[ISI]
Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368376.[ISI][Medline]
. 1991. PHYLYP (phylogeny inference package). Version 3.4. Distributed by the author, Department of Genetics, University of Washington, Seattle.
Fitch, W. M. 1971. Toward defining the course of evolution, minimum change from a specific tree topology. Syst. Zool. 20:406415.[ISI]
Fumagalli, L., P. Taberlet, D. T. Stewart, L. Gielly, J. Hausser, and P. Vogel. 1999. Molecular phylogeny and evolution of Sorex shrews (Soricidae: Insectivora) inferred from mitochondrial DNA sequence data. Mol. Phylogenet. Evol. 11:222235.[ISI][Medline]
Gadaleta, G., G. Pepe, G. de Candia, C. Quagliariello, E. Sbisa, and C. Saccone. 1989. The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: signals revealed by comparative analysis between vertebrates. J. Mol. Evol. 28:497516.[ISI][Medline]
Gissi, C., A. Gullberg, and U. Arnason. 1998. The complete mitochondrial DNA sequence of the rabbit, Oryctolagus cuniculus. Genomics 50:161169.
Gregory, W. K. 1910. The orders of mammals. Bull. Am. Mus. Nat. Hist. 27:1524.
Hasegawa, M., H. Kishino, and T. Yano. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160174.[ISI][Medline]
Hiendleder, S., H. Lewalski, R. Wassmuth, and A. Janke. 1998. The complete mitochondrial DNA sequence of the domestic sheep (Ovis aries) and comparison with the other major ovine haplotype. J. Mol. Evol. 47:441448.[ISI][Medline]
Hutchinson, J. H. 1968. Fossil Talpidae from the later Tertiary of Oregon. Bull. Mus. Nat. Hist. Univ. Oreg. 11:1117.
Janke, A., G. Feldmaier-Fuchs, W. K. Thomas, A. von Haeseler, and S. Pääbo. 1994. The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137:243256.
Janke, A., N. J. Gemmell, G. Feldmaier-Fuchs, A. von Haeseler, and S. Pääbo. 1996. The mitochondrial genome of a monotremethe platypus (Ornithorhynchus anatinus). J. Mol. Evol. 42:153159.[ISI][Medline]
Janke, A., X. Xu, and U. Arnason. 1997. The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogentic relationship among Monotremata, Marsupialia and Eutheria. Proc. Natl. Acad. Sci. USA 94:12761281.
Kim, K. S., S. E. Lee, H. W. Jeong, and J. H. Ha. 1998. The complete nucleotide sequence of the domestic dog (Canis familiaris) mitochondrial genome. Mol. Phylogenet. Evol. 10:210220.[ISI][Medline]
Kishino, H., and M. Hasegawa. 1989. Evaluation of the maximum likelihood estimate of the evolutioary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29:170179.[ISI][Medline]
Kishino, H., T. Miyata, and M. Hasegawa. 1990. Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J. Mol. Evol. 31:153160.
Krettek, A., A. Gullberg, and U. Arnason. 1995. Sequence analysis of the complete mitochondrial DNA molecule of the hedgehog, Erinaceus europaeus, and the phylogenetic position of the Lipotyphla. J. Mol. Evol. 41:952957.[ISI][Medline]
Lavergne, A., E. Douzery, T. Stichler, F. M. Catzeflis, and M. S. Springer. 1996. Interordinal mammalian relationships: evidence for paenungulate monophyly provided by complete mitochondrial 12S rRNA sequences. Mol. Phylogenet. Evol. 6:245258.[ISI][Medline]
Lopez, J. V., M. Culver, S. Cevario, and S. J. OBrien. 1996. Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA repeat (Numt) in the nuclear genome. Genomics 33:229246.
McDowell, S. B. 1958. The Greater Antillean insectivores. Bull. Am. Mus. Nat. Hist. 115:113214.
McKenna, M. C. 1975. Toward a phylogeny and classification of the Mammalia. Pp. 2146 in W. P. Luckett and F. S. Szalay, eds. Phylogeny of the Primates: a multidisciplinary approach. Plenum Press, New York.
McKenna, M. C., and S. K. Bell. 1997. Classification of mammals above the species level. Columbia University Press, New York.
MacPhee, R. D. E., and M. J. Novacek. 1993. Definition and relationships of Lipotyphla. Pp. 1331 in F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds. Mammal phylogeny: placentals. Springer-Verlag, New York.
Novacek, M. J. 1989. Higher mammal phylogeny: the morphological-molecular synthesis. Pp. 421435 in B. Fernholm, K. Bremer, and J. Jörnvall, eds. The hierarchy of life. Elsevier, Amsterdam.
. 1990. Morphology, palaeontology, and the higher clades of mammals. Pp. 507543 in H. H. Genoways, ed. Current mammalogy. Vol. 2. Plenum Press, New York.
. 1992. Mammalian phylogeny: shaking the tree. Nature 356:121125.
Novacek, M. J., and A. R. Wyss. 1986. Higher-level relationships of the recent eutherian orders: morphological evidence. Cladistics 2:257287.
Novacek, M. J., A. A. Wyss, and M. C. McKenna. 1988. The major groups of eutherian mammals. Pp. 3171 in M. J. Benton, ed. The phylogeny and classification of the Tetrapods. Clarendon Press, Oxford, England.
Ohdachi, S., R. Masuda, H. Abe, J. Adachi, N. E. Dokuchaev, V. Haukisalmi, and M. C. Yoshida. 1997. Phylogeny of Eurasian soricine shrews (Insectivora, Mammalia) inferred from the mitochondrial cytochrome b gene sequences. Zool. Sci. 14:527532.[ISI]
Ojala, D., J. Montoya, and G. Attardi. 1990. tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470474.
Penny, D., and M. Hasegawa. 1997. The platypus put in its place. Nature 387:549550.
Pumo, D. E., P. S. Finamore, W. R. Franek, C. J. Carleton, S. Tarzami, and D. Balzarano. 1998. Complete mitochondrial genome of a neotropical fruit bat, Artibeus jamaicensis, and a new hypothesis of the relationships of bats to other eutherian mammals. J. Mol. Evol. 47:709717.[ISI][Medline]
Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406425.[Abstract]
Springer, M. S., G. C. Cleven, O. Madsen, W. W. De Jong, V. G. Waddell, H. M. Amrine, and M. J. Stanhope. 1997. Endemic African mammals shake the phylogenetic tree. Nature 388:6164.
Stanhope, M. J., V. G. Waddell, O. Madsen, W. W. de Jong, S. B. Hedges, G. C. Cleven, D. Kao, and M. S. Springer. 1998. Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. Proc. Natl. Acad. Sci. USA 17:99679972.
Strimmer, K., and A. von Haeseler. 1996. Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13:964969.
Sullivan, J., and D. L. Swofford. 1997. Are guinea pigs rodents? The importance of adequate models in molecular phylogenies. J. Mamm. Evol. 4:7786.
Templeton, A. R. 1983. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to humans and apes. Evolution 37:221244.
Ursing, B. M., and U. Arnason. 1998a. The complete mitochondrial DNA sequence of the pig (Sus scrofa). J. Mol. Evol. 47:302306.
. 1998b. Analyses of mitochondrial genomes strongly support a hippopotamus-whale clade. Proc. R. Soc. Lond. B Biol. Sci. 265:22512255.
Waddell, P. J., Y. Cao, J. Hauf, and M. Hasegawa. 1999. Using novel phylogenetic methods to evaluate mammalian mtDNA, including amino acid-invariant sites-LogDet plus site stripping, to detect internal conflicts in the data, with special reference to the positions of hedgehog, armadillo, and elephant. Syst. Biol. 48:3153.[ISI][Medline]
Werdelin, L., and A. Nilsonne. 1999. The evolution of the scrotum and testicular descent in mammals: a phylogenetic view. J. Theor. Biol. 196:6172.[ISI][Medline]
Xu, X., A. Gullberg, and U. Arnason. 1996. The complete mitochondrial DNA (mtDNA) of the donkey and mtDNA comparisons among four closely related mammalian species-pairs. J. Mol. Evol. 43:438446.[ISI][Medline]
Xu, X., and U. Arnason. 1994. The complete mitochondrial DNA sequence of the horse, Equus caballus; extensive heteroplasmy of the control region. Gene 148:357362.
. 1997. The complete mitochondrial DNA sequence of the white rhinoceros, Ceratotherium simum, and comparison with the mtDNA of the Indian rhinoceros, Rhinoceros unicornis. Mol. Phylogenet. Evol. 7:189194.
Xu, X., A. Janke, and U. Arnason. 1996. The complete mitochondrial DNA sequence of the greater Indian rhinoceros, Rhinoceros unicornis, and the phylogenetic relationship among Carnivora, Perissodactyla, and Artiodactyla (+ Cetacea). Mol. Biol. Evol. 13:11671173.[Abstract]