Phylogeny of the New World true frogs (Rana)

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Abstract

Phylogenetic relationships among the species of true frogs (Rana) from North, South, and Central America were investigated based on the sequences of approximately 2 kb from the mitochondrial genome, sampled from most of the described species, as well as eight undescribed species. This analysis, combined with previous studies of the phylogeny of New World Rana, served as the basis for a revised classification of the group. The American species of Rana are not monophyletic; the western North American Amerana is more closely related to the R. temporaria group of Eurasia (together, these frogs form the group Laurasiarana). The remaining species from the Americas form the monophyletic group Novirana, which includes: R. sylvatica; Aquarana (the R. catesbeiana group); Ranula (the R. palmipes group, including the mostly upland Levirana species and the mostly lowland Lithobates species); Torrentirana (the R. tarahumarae group, or Zweifelia, plus R. sierramadrensis), Stertirana (the R. montezumae group, or Lacusirana, plus R. pipiens), Nenirana (the R. areolata group), and Scurrilirana (most of the southern and tropical leopard frogs). The mitochondrial sequences supported many of the previous hypotheses of relationships of New World Rana, although there were some differences involving the placement of the species R. pipiens, R. sierramadrensis, and R. sylvatica. Parametric bootstrap analyses indicated significant support for the relationships inferred from the mtDNA sequences, and rejected the previous hypotheses of relationships for these three species.

Introduction

The approximately 250 extant species of true frogs (Rana) are found throughout much of the world, with the major exceptions being the polar regions, most of Australia, and the temperate regions of South America. About one-quarter of the species of Rana are found in the Americas, with the largest concentration in the southern United States and Mexico. In the New World, species of Rana are found from Alaska and Canada south throughout the continental United States and all of Middle America to northwestern Peru on the west side of the Andes and to eastern Brazil and northern Bolivia on the east side of the Andes. Collectively, these species are found in almost all of the major biotic provinces that are inhabited by frogs—tundra, temperate coniferous and deciduous forests, grasslands, deserts, brackish-water marshes, freshwater streams and lakes, semitropical cloud forests, and tropical rain forests.

Because one or another species of Rana is common throughout much of the world, several species of Rana have served as research subjects for a broad array of studies in evolution, ecology, behavior, development, genetics, and physiology. Given the large amount of comparative biological information available among species of Rana, this group has great potential for placing a wide range of biological studies in an evolutionary framework, as long as phylogenetic estimates for the group are available. This study examines the phylogeny and diversification of Rana in the New World based on mitochondrial DNA, and tests the significance of differences between current and previous estimates of New World Rana phylogeny. Our goal is to provide a comprehensive and well-supported phylogeny for the group to facilitate comparative studies on the biology of these frogs.

At least three species of New World Rana are thought to have become extinct in historic times, and several of the remaining species have undergone serious declines and are threatened with extinction. Many of the threatened species occur in the western United States and Mexico. In addition, several New World tropical species have not yet been described. This study includes all of the undescribed species of which we are aware. A second goal of this study is to provide the phylogenetic background for a revised classification of the New World Rana. The phylogeny will also be useful for determining priorities for conservation of the biological diversity of New World Rana.

The New World species are thought to form a monophyletic group together with the Rana temporaria species group of Eurasia (Case, 1978a, Farris et al., 1983, Hillis and Davis, 1986, Post and Uzzell, 1981, Wallace et al., 1973), and perhaps other Eurasian species groups as well (Dubois, 1992). These previous studies have supported the placement of the root of the New World Rana tree between the Rana boylii plus Rana temporaria groups in one clade, and the remainder of the New World Rana in the sister clade. Therefore, we used the R. boylii and R. temporaria groups as our outgroups to the remaining species. We included one species in the R. temporaria group in our study, but have otherwise restricted our analysis to the New World species (including most of the species in the R. boylii group). Previous studies of the phylogeny of New World Rana (Case, 1978a, Hillis and Davis, 1986, Hillis et al., 1983, Wallace et al., 1973) have not been comprehensive in the taxa sampled, and the phylogenetic estimates have been based on relatively small data sets. In this study, we attempted to include all extant species of New World Rana (described species, as well as new, but as yet undescribed, species) and examined approximately 2 kb of DNA sequences from three mitochondrial genes (large and small subunits of the ribosomal RNA genes, and the valine tRNA gene). A few described extant species were not available to us for study, but these few species are each thought to be closely related to other species that we did include in our analyses.

Section snippets

Taxon sampling

We collected sequence data from 58 species of Rana, including all the extant described species from the New World except five species of leopard frogs that are closely related to other included species, and two members of the Rana boylii group that are variously treated as species or subspecies. One of the leopard frogs we failed to include was R. megapoda; the sample we collected to represent this species actually represents a related but undescribed species. Hillis et al. (1983) originally

Phylogenetic analysis

The best-fit tree based on the maximum likelihood analysis is shown in Fig. 1, with all branches that have significant support (posterior probability >95%) indicated by asterisks. This tree has a log-likelihood score of −21812.64132. All of the PAUP* and genetic algorithm searches found this tree or another tree of similar but slightly lower score (−21812.66941); this latter tree differed only in rearrangements of some of the weakly supported clades within the tropical leopard frogs (

Relationships of Rana sylvatica

The relationship of Rana sylvatica to other species of the New World Rana has long been controversial. In general appearance, this species resembles species of the R. temporaria group (of Laurasiarana), and many authors have long assumed that R. sylvatica was simply a North American member of this otherwise Eurasian species group. Likewise, Amerana of western North America has been considered to be closely related to, or even a part of, the R. temporaria group (Farris et al., 1980, Farris et

Conclusions

The phylogenetic estimate shown in Fig. 1 provides an opportunity for the comparative study of many aspects of the biology of species of New World Rana. The species in this group are highly diverse in ecology, physiology, and behavior, and many of the species are common enough to be ideal subjects for intensive biological study. As an example, the group as a whole would serve as an excellent model system for the study of many aspects of call evolution in frogs. There is considerable variation

Acknowledgments

We thank Marty Badgett and Todd Schlenke for laboratory assistance. The following people provided some of the tissues samples, assisted in the field, assisted with analyses, made suggestions on the manuscript, or provided other assistance for which we are grateful: Jonathan Campbell, Luis Coloma, Brian Crother, William Duellman, Darrel Frost, John Frost, Jacques Gauthier, Harry Greene, Jeff Jaeger, William Lamar, Julian Lee, Carl Lieb, Paul Moler, James Platz, John Simmons, David Wake, and

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