Mitogenomic relationships of placental mammals and molecular estimates of their divergences

Abstract

Molecular analyses of the relationships of placental mammals have shown a progressive congruence between mitogenomic and nuclear phylogenies. Some inconsistencies have nevertheless persisted, notably with respect to basal divergences. The current study has aimed to extend the representation of groups, whose position in the placental tree has been difficult to establish in mitogenomic studies. Both ML (maximum likelihood) and Bayesian analyses identified four basal monophyletic groups, Afroplacentalia (= Afrotheria: Hyracoidea, Proboscidea, Sirenia, Tenrecidea, Tubulidentata, Macroscelidea, Chrysochloridea), Xenarthra, Archontoglires (Primates, Dermoptera, Scandentia, Lagomorpha, Rodentia) and Laurasiaplacentalia (Lipotyphla, Chiroptera, Pholidota, Carnivora, Perissodactyla, Artiodactyla, Cetacea). All analyses joined Archontoglires and Laurasiaplacentalia on a common branch (Boreoplacentalia), but the relationship between Afroplacentalia, Xenarthra and Boreoplacentalia was not conclusively resolved. The phylogenomic hypothesis with a sister group relationship between Notoplacentalia (Afroplacentalia/Xenarthra) and Boreoplacentalia served as the basis for estimating the times of placental divergences using paleontologically well-supported mammalian calibration points. These estimates placed the basal placental divergence between Boreoplacentalia and Notoplacentalia at ≈ 102 MYA (million years ago). The current estimates of ordinal placental divergences are congruent with recent estimates based on nuclear data, but inconsistent with paleontological notions that have placed the origin of essentially all placental orders within an interval of 5–10 MY in the early Tertiary. Among less deep divergences the estimates placed the split between Gorilla and Pan/Homo at ≈ 11.5 MYA and that between Pan and Homo at ≈ 8 MYA. As a consequence of these estimates, which are in accord with recent progress in primate paleontology, the earliest divergences among recent humans become placed ≈ 270,000 years ago, i.e. ≈ 100,000 years earlier than the traditional age of “Mitochondrial Eve”. Comparison between the two new mt genomes of Hylomys suillus (short-tailed gymnure) patently demonstrates the inconsistency that may exist between taxonomic designations and molecular difference, as the distance between these two supposedly conspecific genomes exceeds that of the three elephantid genera Elephas, Mammuthus and Loxodonta. In accordance with the progressive use of the term Placentalia for extant orders and extinct taxa falling within this group we forward new proposals for the names of some superordinal clades of placental mammals.

Introduction

Mitogenomics, i.e. phylogenetic analyses based on the concatenated aa (amino acid) sequences of proteins or on the nt (nucleotide) sequences of protein-coding genes from complete mitochondrial (mt) genomes, have provided valuable information on mammalian relationships at different levels. The applicability of mt sequences to the examination of phylogenetic relationships is partly due to the unequivocal orthology of these sequences and partly to the facility with which they can be acquired. However, since the amount of data that can be obtained from mt genomes is finite, the conclusive solution to tenuous evolutionary relationships will by necessity rely upon the accumulation of nuclear data. It is nevertheless likely that mitogenomic analyses will still remain valuable for studying phylogenetic relationships in temporal windows within which mt sequences generally provide greater resolution than nuclear data of similar sizes. The maternal inheritance of the mt genome is another feature that makes these genomes valuable, notably for population studies including comparisons with Y chromosomal data.

More than 200 mammalian species are to date represented by complete mt genomes. This collection includes the three extant monotreme species and representatives of all recent orders of both marsupial and placental mammals. In the current mitogenomic study we address phylogenetic questions among placental mammals that have proved contentious, even in analyses of extensive nuclear data. In order to increase the comprehensiveness of the study we have made particular efforts to extend the sampling of basal groups. The phylogenetic questions addressed include (i) the position of the Erinaceidae (hedgehogs and moon rats), (ii) the Epitheria hypothesis, i.e. whether there is a basal split between Xenarthra and other placental orders (= Epitheria, McKenna, 1975), (iii) the support for a basal split between an African clade (Afroplacentalia) and remaining placentals, and (iv) the potential split between Xenarthra/Afroplacentalia (= Notoplacentalia) and other placental orders (Boreoplacentalia).

The sequencing of the mt genome of the hedgehog aimed to determine the position of Lipotyphla in the tree of placental mammals (Krettek et al., 1995). Lipotyphla was at this time recognized as encompassing the families Erinaceidae, Tenrecidae, Chrysochloridae, Solenodontidae, Talpidae and Soricidae (Butler, 1988), an arrangement that is no longer tenable, as two of these families, Tenrecidae and Chrysochloridae, fall within Afroplacentalia. The study of Krettek et al. (1995) showed a basal split between the hedgehog and other placental mammals. This position of Erinaceidae has been maintained in essentially all subsequent mitogenomic studies that have been performed without constraining Erinaceidae to a particular position. Prior to the current study Erinaceidae was represented by the mt genomes of two species, Erinaceus europaeus and Hemiechinus auratus, both included in the Erinaceinae, and one species, Echinosorex gymnurus, belonging to the Hylomyinae. Here we add two specimens of Hylomys suillus (short-tailed gymnure) to the mitogenomic data set, thereby splitting the long Hylomyinae branch in an effort to clarify the position of Erinaceidae. The establishment of this position directly concerns the resolution of basal relationships among placental mammals because mitogenomic analyses have generally tended to promote a basal split between Erinaceidae and remaining taxa.

A variant of the Epitheria hypothesis has postulated a sister group relationship between Xenarthra/Pholidota and remaining eutherians (Novacek, 1992). This notion is inconsistent with mitogenomic results that have placed Pholidota as the probable sister group to Carnivora in an extended Cetferungulata (Arnason et al., 2002, Arnason and Janke, 2002). The number of xenarthran species included in the current analyses exceeds that of previous mitogenomic studies, a circumstance that should promote the identification of the position of Xenarthra in the placental tree and allow improved molecular estimates of the time of basal xenarthran divergences.

The establishment of the monophyly of Rodentia and Glires was for a long time problematic in mitogenomic studies (e.g. D'Erchia et al., 1996, Arnason et al., 2002, Horner et al., 2007) and the currently established tree differs in some crucial respects (e.g. Glires and the positions of Erinaceidae and Primates) from previous mitogenomic trees that served as the basis for molecular estimates of the relationships among placental mammals (Arnason et al., 1996, Arnason et al., 1998, Arnason et al., 2000a, Arnason et al., 2002, Arnason and Janke, 2002). Also hypotheses with either Afroplacentalia or Notoplacentalia as sister to remaining placental mammals have been difficult to distinguish from the Epitheria hypothesis in both mitogenomic and nuclear studies. The current addition of new mt genomes has inter alia aimed to split the hyracoid, sirenian, proboscid and chrysochlorid branches in an effort to establish different nodes within the African clade. The inclusion of these taxa may also help to stabilize the position of Afroplacentalia in the tree of placental mammals. It will at the same time draw attention to an early morphologically based suggestion of phylogenetic affinities between Tubulidentata and Hyracoidea and Proboscidea, suggested by Le Gros Clark and Sonntag (1926).