Mammalian mitogenomic relationships and the root of the eutherian tree

Abstract

Mitogenomic (mtg) phylogenetics has contributed considerably to resolving evolutionary relationships among mammals. However, relatively few genomes have been sequenced for some orders and others are still unrepresented. The first eutherian mtg study (1) included five orders: Rodentia, Primates, Artiodactyla, Cetacea, and Carnivora. This study identified a sister group relationship between Artiodactyla and Cetacea and close affinities between these two orders and Carnivora. Because of the absence of an unequivocal outgroup (OG), the relationships relative to Primates and Rodentia could not be resolved, however. The first mtg rooting of the eutherian tree (2), using a marsupial as OG, reconstructed the relationship OG(Rodentia,(Primates,(Carnivora,(Artiodactyla,Cetacea)))), a topology that has been generally identified in subsequent mtg analyses. These two studies also showed that individual mitochondrial (mt) genes did not obligatorily reconstruct the same topology, underlining the necessity of using the concatenated sequences of different genes for maximizing the reliability of the analyses.

Most taxonomic schemes recognize 18 orders of extant eutherians (Table ​(Table1).1). It is likely, however, that this number is an underestimate because most molecular studies, both mtg (3, 4) and mt/nuclear (5–7), split Lipotyphla into separate lineages. Similarly, if Rodentia is nonmonophyletic (8–11), the number of eutherian orders may be still greater than suggested by only lipotyphlan polyphyly.

Five eutherian orders are previously not represented by complete mtDNAs. To further complete the picture of eutherian mtg relationships we have added 11 complete mtDNAs to the eutherian data set, including four of these orders: Pholidota, Dermoptera, Sirenia, and Macroscelidea.

The phylogenetic position of Pholidota has been a matter of debate. A sister group relationship between Xenarthra and Pholidota in a basal position in the eutherian tree has been proposed (e.g., ref. 12). However, other authors (13) have challenged this proposal. Most morphological studies place Xenarthra at or close to the base of the eutherian tree and the term Epitheria has been coined for all eutherians except Xenarthra (14) or, alternatively, all eutherians except Xenarthra and Pholidota. Thus, the positions of Xenarthra and Pholidota are fundamental to the discussion of eutherian evolution. Xenarthra is currently represented by a single mtDNA, that of the armadillo. To examine the position of Xenarthra on the basis of more comprehensive sequence data we here add the mt genome of the lesser anteater to the mtg data set.

Also, the phylogenetic position of Macroscelidea has been contentious. For example, Simpson (15) joined Macroscelidea and Lipotyphla as sister groups in “Insectivora.” Other morphological proposals have joined Macroscelidea, Lagomorpha, and Rodentia on a common branch, a view endorsed by McKenna and Bell (16), who included this grouping in the Anagalida along with some extinct orders.

The morphological affinities between Proboscidea and Sirenia are well documented (e.g., ref. 17). The mt genome of the dugong allows firmer establishment of the position of Sirenia than was possible in a previous cyt b study (18).

The grouping of Primates, Dermoptera, Scandentia (tree shrews), and Chiroptera (bats) into the superordinal clade Archonta has been favored by morphologists (16). To examine the relationships between Primates and their presumed closest relatives we have added the flying lemur to the mtg sampling. The order Primates includes three basal lineages, Prosimii, Tarsioidea, and Anthropoidea. Anthropoidea is well represented by mtg data, but only one prosimian mt genome (Nycticebus coucang) has been described (19). The addition of the ring-tailed lemur to the data set splits the prosimian branch, allowing extended study of basal primate relationships in conjunction with the recent release of a tarsier sequence.

We add also the mt genomes of the brown hare (Lagomorpha), the tree shrew, the polar bear, the northern sea lion, and the walrus. Lagomorpha is currently represented by the mt genomes of the rabbit and the pika. The brown hare completes the sampling, providing additional data for analysis of the Glires hypothesis, which posits a sister group relationship between Rodentia and Lagomorpha. The phylogenetic position of the Scandentia has been studied (20) but the current taxon sampling has allowed further analysis of its position.

Pinniped relationships are of a particular interest because of the distinct difference between molecular results and recent morphological views (e.g., ref. 21) that posit a sister group relationship between Phocidae and Odobenidae to the exclusion of Otariidae. However, this proposal is inconsistent with chromosomal data (22) and analyses of cyt b and 12S rRNA sequences (23–25). The mtDNAs of the walrus, sea lion, and polar bear allow a firmer analysis of pinniped relationships than was previously possible.

Accession nos. of new mtDNAs are shown in bold. The sequence of the hedgehog has been corrected compared to the original submission. The sequence of the brown rat is from a wild-caught animal. Erinaceomorpha, Tenrecomorpha, and Soricomorpha are traditionally included in the Lipotyphla.

The probability values according to the SH test for alternative relationships relative to the best likelihood tree based on amino acid sequences (Fig. ​(Fig.1)1) are shown next to the differences in log-likelihood values, the number of amino acid substitutions (steps), and their SDs. Anth, Anthropoidea; Art, Artiodactyla; Cet, Cetacea; Derm, Dermoptera; Pro, Prosimii; Tars, Tarsioidea.

A dash (—) indicates that this branch was not or differently resolved. LBP, local bootstrap probability; NJ, neighbor joining; FIT, fitch; MP, maximum parsimony; PUZ, tree-puzzle.

Acknowledgments

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Footnotes