Molecular phylogenetic relationships of moles, shrew moles, and desmans from the new and old worlds

Abstract

A rich variety of anatomical and physiological specializations has enabled members of the family Talpidae (moles, shrew moles, and desmans) to exploit a diverse range of habitats: terrestrial, semi-aquatic, aquatic/fossorial, semi-fossorial, and fossorial. While numerous morphological and biochemical studies pertaining to the origin and radiation of the Talpidae have been completed, phylogenetic hypotheses remain controversial. To address this shortcoming we sequenced the mitochondrial DNA cytochrome b gene (1140 bp) from 29 individuals spanning 12 talpid species. Phylogenetic trees incorporating 12 New and Old World genera (18 species; all 3 extant subfamilies) were then constructed using NJ, MP, ML, and NJ–ML (NJ with ML parameters) methods. Our results provide molecular support for a mononphyletic Talpidae, and suggest that the 12 genera are clustered into seven major clades; (1) Asiatic shrew-like moles (Uropsilus), (2) North American aquatic/fossorial moles (Condylura), (3) North American fossorial moles (Parascalops, Scalopus, and Scapanus), (4) North American semi-fossorial shrew moles (Neurotrichus), (5) Japanese semi-fossorial shrew moles (Dymecodon and Urotrichus), (6) European semi-aquatic desmans (Desmana), and (7) Eurasian fossorial moles (Euroscaptor, Mogera, and Talpa). None of these groupings comprised mole species from both continents. In fact, North American moles and shrew moles do not appear to have specific affinities with Asian moles and shrew moles, respectively. Although low bootstrap support was generally found for evolutionary nodes uniting the major talpid clades, all gene trees constructed identified fossorial North American and Eurasian mole lineages as nonmonophyletic groups, suggesting subterranean specializations arose independently at least twice during the evolution of the Talpidae. Additionally, our data set provides molecular support for a basal divergence and long independent history of Uropsilus from the main talpid line, and refutes the traditional taxonomic status and secondarily basal phylogenetic placement of the subfamily Desmaninae within the Talpidae.

Introduction

The late Tertiary was an important epoch of adaptive radiation and lineage expansion for moles, shrew moles, and desmans of the family Talpidae (Mammalia, Eulipotyphla). During this period, talpids evolved a remarkable variety of locomotor patterns and life history traits including ambulatory (shrew-like moles), semi-aquatic (desmans), aquatic/fossorial (star-nosed mole), semi-fossorial (shrew moles), and highly fossorial (moles in the strict sense) (Hutchison, 1976; Yates and Moore, 1990). Recent classifications recognize anywhere from 12 to 17 genera and 31–42 species (Corbet and Hill, 1991; Nowak, 1999; Yates, 1984) grouped into three extant subfamilies: Uropsilinae (Uropsilus), Desmaninae (Desmana and Galemys), and Talpinae (all remaining genera). The latter subfamily is further subdivided into 5 well-defined tribes; Talpini (Old World fossorial moles), Scalopini (North American fossorial moles), Urotrichini (shrew moles), Scaptonychini (Scaptonyx; long-tailed mole), and Condylurini (Condylura) (McKenna and Bell, 1997).

The oldest fossils assigned to the Talpidae are from late Eocene and late Oligocene sediments of Europe and North America, respectively (McKenna and Bell, 1997). Based on these specimens and geological evidence, it has been suggested that the family originated in Europe and spread by way of multiple dispersal events to Asia and North America (Hutchison, 1976; Moore, 1986; Whidden, 2000). Today, highly fossorial talpids are distributed continuously worldwide from the Eurasian continent, including the Japanese Islands, to North America. Less-fossorial talpids tend to show limited geographic distributions. Desmans, for instance, are limited to drainage basins in north-eastern (Desmana) and north-western (Galemys) Europe, while shrew moles are restricted to Japan (Dymecodon and Urotrichus) and western North America (Neurotrichus). The observation that both living and fossilized talpids exhibit noncontiguous distributions within and between Europe, Asia and North America is a major source of controversy among phylogenetic hypotheses relating to the evolution and radiation of the family (e.g., Hutchison, 1968, Hutchison, 1976; Whidden, 2000; Yates and Moore, 1990). Despite a general lack of phylogenetically informative data, the subfamilies Uropsilinae and Desmaninae are commonly placed at the basal and intermediate nodes, respectively, in cladograms for the family (Whidden, 2000; Yates and Moore, 1990). However, it is the relationships among the ecologically diverse tribes of the subfamily Talpinae that are most contentious.

Based on combined allozymic, chromosomal and morphological data sets, Yates and Moore (1990) recognized two major groups of extant fossorial moles, one from the Old World (Mogera, Euroscaptor, and Talpa) and the other from the New World (Parascalops, Scalopus, and Scapanus) and China (Scapanulus). Interestingly, these authors place semi-fossorial and aquatic/fossorial talpids between these two strictly fossorial tribes. In contrast, Whidden (2000) grouped the fossorial Eurasian (represented by Talpa) and North American moles as a monophyletic, highly derived assemblage based on his study of comparative myology. A monophyletic group of semi-fossorial shrew moles from Japan (Urotrichus and Dymecodon) and North American (Neurotrichus) is also generally supported by studies of osteology (Campbell, 1939; Hutchison, 1976), myology (Whidden, 2000), and cytogenetics and morphology (Moore, 1986; Yates and Moore, 1990). However, studies based on allozymes (Yates and Greenbaum, 1982) and dental homologies (Ziegler, 1971) have raised the possibility that these morphologically similar forms may have arisen separately.

To our knowledge there is no molecular phylogenetic data published for the Talpidae except for two studies limited to seven Eurasian species (Okamoto, 1999; Tsuchiya et al., 2000) and a recent study investigating lipotyphlan relationships that incorporated four talpid genera (Douady et al., 2002). To establish an explicit molecular phylogeny of the Talpidae and hopefully resolve whether semi-aquatic, semi-fossorial and fossorial Eurasian, and North American talpids evolved independently or represent monophyletic assemblages, we conducted a detailed phylogenetic analysis of the mitochondrial DNA cytochrome b (cyt b) gene from 18 species of moles, shrew moles, and desmans from both the New and Old Worlds. Our second goal was to evaluate traditional talpid classification schemes based upon our mtDNA data set.