Phylogeny and Evolutionary History of the Ground Squirrels (Rodentia: Marmotinae)

P1: GXB Journal of Mammalian Evolution (JOMM) PP1059-jomm-4771133 January 27, 2004 11:29 Style file version June 17, 2003 C 2003) Journal of Mammalian Evolution, Vol. 10, No. 3, September 2003 (° Phylogeny and Evolutionary History of the Ground Squirrels (Rodentia: Marmotinae) Richard G. Harrison,1,5 Steven M. Bogdanowicz,1 Robert S. Hoffmann,2 Eric Yensen,3 and Paul W. Sherman4 Although ground squirrels (Spermophilus) and prairie dogs (Cynomys) are among the most intensively studied groups of mammals with respect to their ecology and behavior, a well-resolved phylogeny has not been available to provide a framework for comparative and historical analyses. We used complete mitochondrial cytochrome b sequences to construct a phylogeny that includes all 43 currently recognized species in the two genera, as well as representatives of two closely related genera (Marmota and Ammospermophilus). In addition, divergence times for ground squirrel lineages were estimated using Bayesian techniques that do not assume a molecular clock. All methods of phylogenetic analysis recovered the same major clades, and showed the genus Spermophilus to be paraphyletic with respect to both Marmota and Cynomys. Not only is the phylogeny at odds with previous hypotheses of ground squirrel relationships, but it suggests that convergence in morphology has been a common theme in ground squirrel evolution. A well-supported basal clade, including Ammospermophilus and two species in the subgenus Otospermophilus, diverged from all other ground squirrels an estimated 17.5 million years ago. Between 10 and 14 million years ago, a relatively rapid diversification gave rise to lineages leading to marmots and to several distinct groups of ground squirrels. The Eurasian ground squirrels diverged from their North American relatives during this period, far earlier than previously hypothesized. This period of diversification corresponded to warming climate and spread of grasslands in western North America and Eurasia. Close geographic proximity of related forms suggests that most species evolved in or near their current ranges. KEY WORDS: ground squirrels, prairie dogs, phylogeny, mtDNA, cytochrome b, molecular clock. INTRODUCTION Ground squirrels (Spermophilus), prairie dogs (Cynomys), and their relatives are among the most intensively studied groups of mammals with respect to their ecology and behavior. Studies of these rodents have enhanced our understanding of the adaptive significance 1 Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York, USA. of Vertebrate Zoology, Division of Mammals, Smithsonian Institution, Washington, District of Columbia, USA. 3 Biology Department, Albertson College, Caldwell, Idaho, USA. 4 Department of Neurobiology and Behavior, Mudd Hall, Cornell University, Ithaca, New York, USA. 5 To whom correspondence should be addressed at Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, New York 14853, USA. E-mail: . 2 Department 249 C 2003 Plenum Publishing Corporation 1064-7554/03/0900-0249/0 ° P1: GXB Journal of Mammalian Evolution (JOMM) 250 PP1059-jomm-4771133 January 27, 2004 11:29 Style file version June 17, 2003 Harrison, Bogdanowicz, Hoffmann, Yensen, and Sherman of hibernation physiology, foraging ecology, predator avoidance behavior, mating behavior, kin discrimination, and social behavior (e.g., Sherman, 1977; Murie and Michener, 1984; Hoogland, 1995; Lacey et al., 1997; Holmes, 2001; Yensen and Sherman, 2003). Ground-dwelling squirrels [including chipmunks (Tamias), marmots (Marmota), and antelope ground squirrels (Ammospermophilus)] vary dramatically in demography (Elliot, 1978; Sherman and Morton, 1984; Van Horne et al., 1997; Schwartz et al., 1998; Sherman and Runge, 2002) and in social organization, which ranges from solitary (13-lined ground squirrel [S. tridecemlineatus], woodchuck [M. monax]) to complex sociality and coloniality (black-tailed prairie dog [C. ludovicianus], Olympic marmot [M. olympus]) (Armitage, 1981; Michener, 1983; Barash, 1989; Schwagmeyer, 1990; Blumstein and Armitage, 1999). Although morphological, ecological, karyological, and biochemical traits have been used to hypothesize evolutionary relationships of some taxa, these studies have generally provided poor resolution or have yielded disparate and sometimes conflicting results (Bryant, 1945; Durrant and Hansen, 1954; Nadler, 1966; Nadler et al., 1971a,b, 1982, 1984; Hafner, 1984; MacNeil and Strobeck, 1987; Stangl and Grimes, 1987; Thomas and Martin, 1993; Goodwin, 1995; Giboulet et al., 1997). The absence of a well-resolved and supported phylogeny has frustrated attempts to test hypotheses for the origin and evolutionary history of morphological, physiological, or behavioral traits in ground-dwelling squirrels (Dobson, 1984; Blumstein and Armitage, 1997, 1998). Spermophilus species are Holarctic in distribution, ranging across Eurasia, from Austria to eastern Siberia, and throughout western North America from Alaska to Mexico, and east as far as Ohio (Hall, 1981; Hoffmann et al., 1993). They occupy a broad range of habitats, including tropical deciduous forests, hot and cold deserts, prairie and steppe, tundra, and woodlands (Howell, 1938; Nadler et al., 1982; Yensen and Valdés-Alarcón, 1999; Wilson and Ruff, 1999). Currently, the genus comprises 38 recognized species, grouped into six subgenera: Otospermophilus, Callospermophilus, Xerospermophilus, Ictidomys, Poliocitellus, and Spermophilus (Hoffmann et al., 1993). According to Bryant (1945), the subgenera form a “graded series” with Otospermophilus and Callospermophilus retaining many ancestral character states, and squirrels in the subgenus Spermophilus representing the most derived (“specialized”) condition. Each subgenus is typically associated with and adapted to a narrow range of environments and plant communities (Howell, 1938; Hafner, 1984). All six subgenera occur in North America, but according to most specialists only members of the subgenus Spermophilus are found in Eurasia, although some authors recognize two additional subgenera (Colobotis and Urocitellus, e.g., Gromov et al., 1965). The five Cynomys species are restricted to the Great Plains and intermontane regions of western North America (Hoffmann et al., 1993). In skull and dentition, Cynomys are very similar to ground squirrels in the subgenus Spermophilus (Bryant, 1945), and a cladistic analysis of morphological traits places Cynomys within the subgenus Spermophilus as part of the crown group within the ground squirrel radiation (Goodwin, 1995). The 14 species of marmots (Marmota) are giant ground squirrels, also Holarctic in distribution, with eight species in Eurasia, ranging from western Europe to eastern Siberia, and six species in North America, from northwestern Alaska south and east to California and Georgia. Marmots are clearly a monophyletic group (Steppan et al. (...truncated)