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Historical Biogeography of Lowland Species of Toads (Bufo) Across The Journal of Biogeography (J. Biogeogr.) (2006) 33, 1889–1904 ORIGINAL Historical biogeography of lowland ARTICLE species of toads (Bufo) across the Trans- Mexican Neovolcanic Belt and the Isthmus of Tehuantepec Daniel G. Mulcahy*, Benson H. Morrill and Joseph R. Mendelson III Department of Biology, Utah State University, ABSTRACT Logan, UT, USA Aim In this study, we investigate phylogeographic structure in two different species groups of lowland toads. First, we further investigate strict parapatry of the Pliocene-vicariant Bufo valliceps/B. nebulifer species pair. Secondly, we test for similar phylogeographic structure in the distantly related toad B. marinus,a species we hypothesize will show a Pleistocene dispersal across the same area. Location The eastern extension of the Trans-Mexican Neovolcanic Belt (TMNB) contacts the Atlantic Coast in central Veracruz, Mexico. Although it is not a massive structure at this eastern terminus, the TMNB has nonetheless effected vicariance and subsequent speciation in several groups of animals. The Isthmus of Tehuantepec unites the North American continent with Nuclear Central America and is also known to be a biogeographic barrier for many taxa. Methods We use sequence data from two mitochondrial DNA genes (c. 550 base-pairs (bp) of 16S and c. 420 bp of cyt b) from 58 individuals of the B. valliceps/nebulifer complex, collected from 24 localities. We also present homologous sequence data from 23 individuals of B. marinus, collected from 12 localities. We conduct maximum-parsimony, maximum-likelihood and Bayesian analyses to investigate phylogeographic structure. We then use parsimony- and likelihood-based topology tests to assess alternative phylogenetic hypotheses and use a previously calibrated molecular rate of evolution to estimate dates of divergence. Results Our results further define the parapatric contact zone across the TMNB between the Pliocene-vicariant sister species B. valliceps and B. nebulifer.In contrast, phylogenetic structure among populations of B. marinus across the TMNB is much shallower, suggesting a more recent Pleistocene dispersal in this species. In addition, we found phylogeographic structure associated with the Isthmus of Tehuantepec in both species groups. Main conclusions The existence of a Pliocene–Pleistocene seaway across the Isthmus of Tehuantepec has been controversial. Our data depict clades on either side of the isthmus within two distinct species (B. valliceps and B. marinus), although none of the clades associated with the isthmus, for either species, are *Correspondence: Daniel G. Mulcahy, reciprocally monophyletic. In the B. valliceps/B. nebulifer complex, the TMNB Department of Herpetology, California separation appears to predate the isthmian break, whereas in B. marinus dispersal Academy of Sciences, 875 Howard Street, San across the TMNB has occurred subsequent to the presence of a barrier at the Francisco, CA 94103-3009, USA. E-mail: [email protected] Isthmus of Tehuantepec. Present address: Department of Herpetology, Keywords Zoo Atlanta, 800 Cherokee Ave SE, Atlanta, GA Bufo nebulifer, Bufo marinus, Bufo valliceps, Bufonids, Central America, Mex- 30315-1440, USA. ico, mitochondrial DNA, phylogeography. ª 2006 The Authors www.blackwellpublishing.com/jbi 1889 Journal compilation ª 2006 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2006.01546.x D. G. Mulcahy, B. H. Morrill and J. R. Mendelson III state of Veracruz, Mexico (Fig. 2). The imposing backbone of INTRODUCTION the TMNB began activity during the mid-Miocene to Pliocene The Trans-Mexico Neovolcanic Belt (TMNB) is one of the (de Cserna, 1989), with its greatest development during the predominant geographical features of Mexico, and its geolo- Pliocene in the eastern portion (Ferrusquia-Villafranca, 1993), gical development has been posited as a primary contributor to giving rise to the highest peaks of Mexico. However, the the biogeographic histories of many upland taxa in central easternmost fingers of the TMNB, where they contact the Gulf Mexico (e.g. Campbell & Frost, 1993; Darda, 1994; Sullivan of Mexico, are barely noticeable to the casual observer. During et al., 2000; Castoe et al., 2003). However, a recent series of much of the Pliocene, sea-level maxima caused by a warmer papers have independently demonstrated the considerable climate effectively covered the entire coastal plain of eastern influence of this transverse massif on the biogeography and Mexico (Bryant et al., 1991). Later during the Pleistocene, sea evolution of the lowland fauna on both the Pacific (Mateos, levels fluctuated with corresponding glacial and inter-glacial 2005) and the Atlantic coasts of Mexico (Mulcahy & cycles (Beard et al., 1982). Glacial-maxima lowered sea levels Mendelson, 2000; Hulsey et al., 2004; Zaldı´var-Rivero´n et al., exposing large sections of the continental shelf, which greatly 2004). These papers generally support earlier hypotheses based increased the aerial extent of the coastal plain (Fig. 1), whereas on observations of consistent disjunctions in the distribution glacial minima raised sea levels, inundating much of the coastal of fishes (Rosen, 1978), and of reptiles and mammals (Pe´rez- plain by about 300 m (Ewing & Lopez, 1991). The area of the Higareda & Navarro, 1980), specifically along the Atlantic Sierra de Los Tuxtlas (Fig. 1) is of volcanic origin from the late Versant of Mexico. Therefore, it is suggested that the TMNB Cenozoic (Ferrusquia-Villafranca, 1993), and may have been may form a common geographical barrier to lowland species in isolated from the mainland during the Pliocene and during this region. Pleistocene glacial minima. Farther south, debate continues as The concept of a massive volcanic chain such as the TMNB to whether a seaway existed at the Isthmus of Tehuantepec, acting as a vicariant feature to lowland populations is easily separating northern Mexico from Nuclear Central America tractable, but the reality is that the TMNB withers to a tiny (Campbell, 1999). string of lava-rock strewn hills at its eastern terminus (Fig. 1). By comparing phylogenetic structure from mtDNA It makes final contact with the current coastline, as a series of sequences of lowland toads in this region, Mulcahy & small fingers of raised lava-rock (the northern-most being just Mendelson (2000) demonstrated that the prevailing concept south of the small town of Palma Sola, the southern-most just of a single wide-ranging species (Bufo valliceps Wiegmann) north of the city Cardel, with a small pocket of suitable habitat should be replaced by recognition of a species pair showing an occurring in the middle, near the town of El Viejo´n) all in the apparent parapatric distribution in the region: B. valliceps Figure 1 Map of the study area, showing major geographic features discussed in the text. Grey shading from light to dark indicates elevations from 300–900 m, 900–2100 m and > 2100 (including black) m a.s.l., respectively. Dotted line shows extent of continental shelf, much of which was exposed during lower sea levels of the Pleistocene (from Bryant & Bryant, 1991). 1890 Journal of Biogeography 33, 1889–1904 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd Biogeography of lowland toads (Bufo) The three species of toads in our study are ecologically similar in their general reproductive biology and overall natural history. All three species are invasive, ‘weedy’ species that are typically more abundant in secondary, degraded habitats than in undisturbed primary forests (Zug & Zug, 1979; Mendelson, 1994; Lee, 1996; Campbell, 1998; McCranie & Wilson, 2002; Savage, 2002). These attributes would suggest that they are suitably comparable to one another, in order to test hypotheses of historical biogeography and that their invasive, dispersal-prone tendencies would make them a conservative test of the effect of the TMNB on lowland species. In this paper, we use c. 970 base-pairs (bp) of sequence data from two mtDNA genes (cyt b and 16S) from recently collected samples along a geographic transect across the TMNB to address the historical biogeography of the Atlantic Versant lowlands of Mexico. Specifically, we test three main hypotheses Figure 2 Map of the eastern terminus of the Trans-Mexico Neovolcanic Belt (TMNB) in central Veracruz. Squares indicate regarding the relationships and distributions concerning reference towns used in text, circles indicate collecting localities for bufonid toads in this region: (1) the hypothesis that B. valliceps Bufo nebulifer (Mx8) B. valliceps (Mx9–10) and B. marinus (Mx8– and B. nebulifer are parapatric at the eastern terminus of the 10) in relation to the eastern-most portion of the TMNB (see TMNB (i.e. as proposed by Mulcahy & Mendelson, 2000); (2) Figs 3 & 4 for complete sampling of each taxon). Shaded contours the hypothesis that the sympatric toad B. marinus shows a indicate elevation following Fig. 1. Los Tuxtlas is the Pliocene pattern of more recent dispersal across the TMNB, consistent volcanic uplift on the coastal plain south of the eastern terminus of with the Pleistocene dispersal, followed by the vicariance the TMNB (see Discussion). hypothesis of Mulcahy & Mendelson (2000); and (3) the hypothesis that there is evidence of a phylogeographic signal within B. valliceps and/or B. marinus, which is consistent with ranging from central Veracruz, Mexico, southward to Costa a historical seaway across the Isthmus of Tehuantepec. We use Rica; and B. nebulifer Girard, ranging from central Veracruz both parsimony and likelihood
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