Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals - PubMed (original) (raw)

Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals

Hidenori Nishihara et al. Proc Natl Acad Sci U S A. 2009.

Abstract

As a consequence of recent developments in molecular phylogenomics, all extant orders of placental mammals have been grouped into 3 lineages: Afrotheria, Xenarthra, and Boreotheria, which originated in Africa, South America, and Laurasia, respectively. Despite this advancement, the order of divergence of these 3 lineages remains unresolved. Here, we performed extensive retroposon analysis with mammalian genomic data. Surprisingly, we identified a similar number of informative retroposon loci that support each of 3 possible phylogenetic hypotheses: the basal position for Afrotheria (22 loci), Xenarthra (25 loci), and Boreotheria (21 loci). This result indicates that the divergence of the placental common ancestor into the 3 lineages occurred nearly simultaneously. Thus, we examined whether these molecular data could be integrated into the geological context by incorporating recent geological data. We obtained firm evidence that complete separation of Gondwana into Africa and South America occurred 120 +/- 10 Ma. Accordingly, the previous reported time frame (division of Pangea into Gondwana and Laurasia at 148-138 Ma and division of Gondwana at 105 Ma) cannot be used to validate mammalian divergence order. Instead, we use our retroposon results and the recent geological data to propose that near-simultaneous divisions of continents leading to isolated Africa, South America, and Laurasia caused nearly concomitant divergence of the ancient placental ancestor into 3 lineages, Afrotheria, Xenarthra, and Boreotheria, approximately 120 Ma.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Placental mammalian tree and 3 phylogenetic hypotheses of major lineages. (A) Mammalian interordinal phylogeny previously analyzed by retroposon insertion analysis (6) with the time scale (53). The bold vertical line denotes the root of placental mammals that was addressed in this study. (B) Three phylogenetic hypotheses to root the eutherian tree: tree 1, Exafroplacentalia (Afrotheria basal); tree 2, Epitheria (Xenarthra basal); and tree 3, Atlantogenata (Boreotheria basal).

Fig. 2.

Fig. 2.

Three examples of L1 insertion loci supporting tree 1 (A), tree 2 (B), and tree 3 (C). Black and gray boxes denote the L1 and the TSD sequences, respectively. The latter were generated during L1 integration and indicate bona fide retrotransposition. The central region of the inserted L1 sequence has been omitted.

Fig. 3.

Fig. 3.

A revised paleogeographic scenario based on recent geological data. (A–C) Paleogeographic reconstruction of Pangea at 146 Ma (A), 120 Ma (B), and 90 Ma (C) (modified after refs. – and 52). (D) A magnified map at 120 Ma (boxed area in B) is shown emphasizing 2 bridges that connect 3 continents. Blue and light blue represent deep and shallow ocean depths, respectively. Brown areas and the yellow jagged line represent landmasses and the mid-Atlantic ridge, respectively. Only deep ocean is represented for Laurasia because drilling data are currently unavailable. (E) Sea-level rise (54) to yield subsequent fragmentation of Africa and South America was taken into consideration for the reconstruction.

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