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Evolutionary History of the Genus Rhamdia (Teleostei: Pimelodidae) in Central America

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Evolutionary History of the Genus Rhamdia (Teleostei: Pimelodidae) in Central America MOLECULAR PHYLOGENETICS AND EVOLUTION Molecular Phylogenetics and Evolution 25 (2002) 172–189 www.academicpress.com Evolutionary history of the genus Rhamdia (Teleostei: Pimelodidae) in Central America Anabel Perdices,a,b,* Eldredge Bermingham,a Antonia Montilla,b and Ignacio Doadriob a Smithsonian Tropical Research Institute, Apto. 2072, Balboa, Republic of Panama b Museo Nacional de Ciencias Naturales, CSIC, Jose Gutierrez Abascal 2, 28006 Madrid, Spain Received 11 June 2001; received in revised form 2 January 2002 Abstract We constructed phylogenetic hypotheses for Mesoamerican Rhamdia, the only genus of primary freshwater fish represented by sympatric species across Central America. Phylogenetic relationships were inferred from analysis of 1990 base pairs (bp) of mito- chondrial DNA (mtDNA), represented by the complete nucleotide sequences of the cytochrome b (cyt b) and the ATP synthase 8 and 6 (ATPase 8/6) genes. We sequenced 120 individuals from 53 drainages to provide a comprehensive geographic picture of Central American Rhamdia systematics and phylogeography. Phylogeographic analysis distinguished multiple Rhamdia mtDNA lineages, and the geographic congruence across evolutionarily independent Rhamdia clades indicated that vicariance has played a strong role in the Mesoamerican diversification of this genus. Phylogenetic analyses of species-level relationships provide strong support for the monophyly of a trans-Andean clade of three evolutionarily equivalent Rhamdia taxa: R. guatemalensis, R. laticauda, and R. ciner- ascens. Application of fish-based mitochondrial DNA clocks ticking at 1.3–1.5% sequence divergence per million years (Ma), suggests that the split between cis- and trans-Andean Rhamdia extends back about 8 Ma, and the three distinct trans-Andean Rhamdia clades split about 6 Ma ago. Thus the mtDNA divergence observed between cis- and trans-Andean Rhamdia species is too low to support an ancient colonization of Central America in the Late Cretaceous or Paleocene as had been hypothesized in one colonization model for Mesoamerican fishes. Rather the mtDNA data indicate that Rhamdia most likely colonized Central America in the late Miocene or Pliocene, promoting a strong role for the Isthmus of Panama in the Mesoamerican expansion of this genus. Basal polytomies suggest that both the R. laticauda and R. guatemalensis clades spread rapidly across the Central American landscape, but differences in the average mtDNA genetic distances among clades comprising the two species, indicate that the R. laticauda spread and diversified across Mesoamerica about 1 million years before R. guatemalensis. Ó 2002 Elsevier Science (USA). All rights reserved. Keywords: Catfishes; Neotropical freshwater fishes; Mitochondrial DNA; ATP synthase; Cytochrome b; Phylogeography; Molecular systematics 1. Introduction only primary freshwater fish genus having sympatrically distributed species north of Panamaais Rhamdia, but in The primary freshwater fish fauna of Central Amer- the absence of a phylogeny for this group one cannot ica stands in stark contrast to the South American fauna determine if these species represent an autochthonous owing to the lack of sympatrically distributed conge- radiation or independent colonizations of Central neric taxa. The generally depauperate nature of the America from South America. Thus, a principal aim of Mesoamerican fish fauna indicates an absence of adap- this paper is to provide a phylogenetic hypothesis for tive radiation, perhaps owing to the relatively short Rhamdia to infer its history in Central America. Fur- period of time since primary Neotropical fishes have thermore, because Rhamdia is comprised of multiple colonized Central America (Bermingham and Martin, evolutionary lineages, the genus offers an unusual op- 1998; Miller, 1966; but see Bussing, 1976, 1975). The portunity to study the timing of colonization, and the subsequent rate of dispersal and diversification across the Central American landscape. * Corresponding author. Fax: +507-2128790. The present study draws upon Silfvergrip’s (1996) E-mail address: [email protected] (A. Perdices). revision of Rhamdia in which the roughly 100 nominal 1055-7903/02/$ - see front matter Ó 2002 Elsevier Science (USA). All rights reserved. PII: S1055-7903(02)00224-5 A. Perdices et al. / Molecular Phylogenetics and Evolution 25 (2002) 172–189 173 species included in the genus were examined and real- which specifically ignored Silfvergrip’s revision of the located to 11 species representing the genera’s broad genus including his well supported statements concern- Neotropical distribution, extending from Meexico to ing conspecific morphological variation, in favor of Argentina. Silfvergrip touched on points that hold drawing attention to the population’s cave-dwelling general interest for systematists and particular relevance natural history. for our more confined study of Rhamdia molecular An apparently simple resolution to the nomenclatural systematics. First, in his morphological analysis of conflict resulting from the lack of sufficient diagnostic Rhamdia quelen, resulting in the synonymy of roughly 40 characters is the collection of more data. In the case of nominal species, Silfvergrip noted ‘‘that different popu- Rhamdia, as we show beyond, mitochondrial DNA lations can be diagnosed successfully if, but only if, a (mtDNA) data permit an objective and character-rich small number of specimens from two sufficiently wide- analysis of the evolutionary distinctiveness of Central spread populations are compared. Once a larger mate- American species and geographic populations. The rial with few ‘geographic gaps’ is filled in, apparent classification dilemma, however, is less easily dis- differences between distant populations disappear and a patched. Thus we utilize our phylogeny of Rhamdia to wide range of character state overlaps emerge.’’ The lack touch upon the classification of phylogenetic lineages of suitable reference material across ‘geographic gaps,’ across Central America, and the importance of classifi- or the absence of systematic analysis of available spec- cation for synthetic studies of the evolutionary and imens, is a general problem when considering the syst- ecological processes that underlie patterns of diversity. ematics of tropical organisms (see, for example, Weitzman and Palmer, 1997). In other words, whether 1.1. Systematic background one compares such things as the behaviors or geo- graphic distributions of tropical taxa, one needs to Silfvergrip’s (1996) revision of the genus Rhamdia question how well current taxonomy describes the evo- (family Pimelodidae) identifies three Central American lutionary distinctiveness and relationships of the taxa species, R. laticauda, R. nicaraguensis,andR. quelen studied. ( ¼ R. guatemalensis and related species of all previous Second, Silfvergrip noted that traditional Rhamdia Central American descriptions), whereas other treat- systematics is more efficient than phylogenetic syste- ments have recognized more than 13 Mesoamerican matics in constructing a classification owing to a much species (Behre, 1928; Bussing, 1975, 1998; Dahl, 1971; less restrictive use of characters in the former. Of course, Espinosa et al., 1993; Greenfield and Thomerson, 1997; efficiency does not replace veracity, which led Silfvergrip Hildebrand, 1938; Loftin, 1965; Martin, 1969; Meek and to emphasize the fact that most Rhamdia species had Hildebrand, 1916; Miles, 1947; Miller, 1984; Weber and been diagnosed using elimination methods based on Wilkens, 1998). Silfvergrip’s R. laticauda and R. quelen dichotomous identification keys. Thus, in his reappraisal are widespread along both the Pacific and Caribbean of the genus he eliminated emphasis on characters that slopes of Central America, although the former is re- he determined were not useful cladistic characters, al- stricted to Central America, while the latter is found though he made no subsequent attempt to phylogenet- throughout South America (Silfvergrip, 1996, Figs. 19 ically analyze Rhamdia species relationships. Here again, and 23). R. nicaraguensis is known only from Nicaragua Rhamdia systematics identifies a general problem con- and Costa Rica (Bussing, 1998, Map 11; Silfvergrip, fronting Neotropical ichthyology. The prevailing tax- 1996, Fig. 20). R. laticauda and R. nicaraguensis are onomy of Neotropical fishes relies to a large extent on often associated with highland or more swiftly running morphometric and meristic characters that overlap in streams, whereas R. quelen is the more abundant low- value between named species. Although there is a strong land form (Bussing, 1998; Silfvergrip, 1996; Villa, 1975). body of careful cladistic analysis of Neotropical fishes, Included in our phylogenetic analyses are five species this is generally carried out at higher taxonomic levels that have been reassigned by Silfvergrip (1996) to (e.g., Bockmann, 1994; Buckup, 1993; Vari, 1995; We- R. laticauda, at least four species that he considers junior itzman et al., 1988). At present there are very few synonyms of R. quelen (including R. guatemalensis), and morphological studies at the level of the genus and be- R. nicaraguensis (Appendix A, Fig. 1). Mexican Rham- low that provide a sufficient number of characters for dia represent some of the best-studied members of the thorough interpretation of species identity and rela- group and exemplify the different taxonomic viewpoints tionship. Conflict arises when subjective taxonomic de- among authors. In Meexico, R. quelen ( ¼ guatemalensis) scription,
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