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STANHOPE, M. J., WADDELL, V. G. et al. (1998)

STANHOPE, M. J., WADDELL, V. G., MADSEN, O., DE JONG, W., BLAIR HEDGES, S., CLEVEN, G. C. , KAO, D. & SPRINGER, M. S. (1998)

Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. 

PNAS 95 (17): 9967–9972. doi: 10.1073/pnas.95.17.9967.

Abstract: 

The traditional views regarding the mammalian order Insectivora are that the group descended from a single common ancestor and that it is comprised of the following families: Soricidae (shrews), Tenrecidae (tenrecs), Solenodontidae (solenodons), Talpidae (moles), Erinaceidae (hedgehogs and gymnures), and Chrysochloridae (golden moles). Here we present a molecular analysis that includes representatives of all six families of insectivores, as well as 37 other taxa representing marsupials, monotremes, and all but two orders of placental mammals. These data come from complete sequences of the mitochondrial 12S rRNA, tRNA-Valine, and 16S rRNA genes (2.6 kb). A wide range of different methods of phylogenetic analysis groups the tenrecs and golden moles (both endemic to Africa) in an all-African superordinal clade comprised of elephants, sirenians, hyracoids, aardvark, and elephant shrews, to the exclusion of the other four remaining families of insectivores. Statistical analyses reject the idea of a monophyletic Insectivora as well as traditional concepts of the insectivore suborder Soricomorpha. These findings are supported by sequence analyses of several nuclear genes presented here: vWF, A2AB, and α-β hemoglobin. These results require that the order Insectivora be partitioned and that the two African families (golden moles and tenrecs) be placed in a new order. The African superordinal clade now includes six orders of placental mammals.

Throughout most of this century, the placental (eutherian) mammals with extant representation have been classified into 18 orders. During this period, the order Insectivora has been among the least stable higher taxa in Eutheria, both in terms of phylogenetic position and taxonomic content. Beginning with Huxley (1) and later embellished by Mathew (2), insectivores have been thought to possess features that rendered them closer to the ancestral stock of mammals. Despite this presumed central position of insectivores in the evolutionary history of mammals, the composition of the group never has been widely agreed on. The prevalent morphological view (3) suggests that the following extant families of “insectivores” descended from a single common ancestor and as such should be those groups that are regarded as the constituents of the order Insectivora (Lipotyphla): Soricidae (shrews), Tenrecidae (tenrecs), Solenodontidae (solenodons), Talpidae (moles), Erinaceidae (hedgehogs and gymnures), and Chrysochloridae (golden moles).

Butler (4) listed six morphological characteristics that, in his opinion, supported a monophyletic Insectivora including (i) absence of cecum; (ii) reduction of pubic symphysis; (iii) maxillary expansion within orbit, displacing palatine; (iv) mobile proboscis; (v) reduction of jugal; and (vi) hemochorial placenta. More recently, MacPhee and Novacek (3) have reviewed the evidence and concluded that characteristics (i) and (ii) support lipotyphlan monophyly, characteristic (iii) possibly does, and (iv–vi), as currently defined, do not, leaving two to three characteristics that, in their opinion, support the order Insectivora.

The six families of insectivores are most often grouped into two clades of subordinal rank: the Erinaceomorpha (hedgehogs) and the Soricomorpha (all other families). Within the Soricomorpha, Butler (4) suggested that the golden moles and tenrecs form a clade and that moles and shrews cluster together, followed by solenodons. MacPhee and Novacek (3), however, proposed three clades of subordinal rank: Chrysochloromorpha (Chrysochloridae), Erinaceomorpha (Erinaceidae), and Soricomorpha (Soricidae, Talpidae, Solenodontidae, and Tenrecidae). This latter organization is based on their view that the Chrysochloridae is “spectacularly autapomorphic.” In their opinion, golden moles show no shared derived traits with the soricomorphs and therefore should be separated from that suborder. This recommendation echoes earlier views regarding the group that have suggested that golden moles are a separate order or suborder (5–7).

A recent molecular study of mammalian phylogeny, which included three insectivore families, demonstrated that golden moles are not part of the Insectivora but instead belong to a clade of endemic African mammals that also includes elephants, hyraxes, sea cows, aardvarks, and elephant shrews (8). Evidence for this now comes from a wide range of disparate molecular loci including the nuclear AQP2, vWF, and A2AB genes as well as the mitochondrial 12S–16S rRNA genes (8, 9). The fossil record of golden moles indicates that the geographic distribution of this group has been restricted to Africa throughout its temporal range (10, 11). The fossil record of tenrecs also suggests an African origin (10, 11). This paleontological record, along with the morphological study of Butler (4), suggests a possible common ancestry for golden moles and tenrecs. However, it also may be that the autapomorphic qualities of golden moles reflect their evolutionary history as a singular distinct lineage of African insectivores, separate from the rest of the order. At present, there is no published molecular phylogenetic perspective on the evolutionary history of the Tenrecidae, there is no molecular study that includes a representative from all families of insectivores, and there are no molecular sequence data (data banks or published accounts) for solenodons.

Here, we report a molecular phylogenetic analysis involving all families of insectivores, using complete sequences of the mitochondrial 12S rRNA, 16S rRNA, and tRNA-Valine genes. These data, along with additional sequences from four disparate nuclear genes, are used to examine the extent of insectivore paraphyly or polyphyly, the conflicting hypotheses regarding the origin of the family Tenrecidae, and the possibility of an African clade of insectivores.

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