Multilocus Phylogeny and Rapid Radiations in Neotropical Cichlid Fishes
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Molecular Phylogenetics and Evolution 55 (2010) 1070–1086 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Multilocus phylogeny and rapid radiations in Neotropical cichlid fishes (Perciformes: Cichlidae: Cichlinae) Hernán López-Fernández a,b,*, Kirk O. Winemiller c, Rodney L. Honeycutt d a Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario, Canada M5S 2C6 b Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario, Canada M5S 3B2 c Section of Ecology, Evolution and Systematic Biology, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843-2258, USA d Natural Science Division, Pepperdine University, 24255 Pacific Coast Hwy., Malibu, CA 90263, USA article info abstract Article history: Neotropical cichlid fishes comprise approximately 60 genera and at least 600 species, but despite this Received 14 September 2009 diversity, their phylogeny is only partially understood, which limits taxonomic, ecological and evolution- Revised 11 February 2010 ary research. We report the largest molecular phylogeny of Neotropical cichlids produced to date, com- Accepted 16 February 2010 bining data from three mitochondrial and two nuclear markers for 57 named genera and 154 species Available online 21 February 2010 from South and Central America. Neotropical cichlids (subfamily Cichlinae) were strongly monophyletic and were grouped into two main clades in which the genera Retroculus (Tribe Retroculini) and Cichla Keywords: (Cichlini) were sister to a monophyletic group containing all other lineages. This group included the Neotropical cichlids tribes Chaetobranchini, Astronotini, Geophagini, Cichlasomatini and Heroini. Topological comparisons Molecular phylogeny South America with previously published hypotheses indicated that our results are congruent with recent analyses of Central America the tribe Cichlasomatini, but significantly more likely than published hypotheses for Geophagini, Heroini Taxonomy and the entire Cichlinae. Improved resolution and support are attributed to increased taxon sampling and Adaptive radiation to the addition of taxa never before included in phylogenetic analyses. Geophagini included two major subclades congruent with our own previous findings but more strongly supported; we also found a new and strongly supported sister-group relationship between Guianacara and Mazarunia. Cichlasomatini relationships were similar to recently proposed topologies, but contrastingly, we found a monophyletic Cichlasoma and support for a monophyletic grouping of the Aequidens diadema and A. tetramerus groups. Three basal South American Heroini lineages were recovered: (Hypselecara + Hoplarchus), Pterophyllum, and a grouping we refer to as mesonautines. Three other South American clades, caquetaines, Australoh- eros and the ‘Cichlasoma’ festae group, were nested within Central American clades. Most Heroini diver- sity was divided into two relatively well-supported large groups: the Southern Central American Clade, including clades herein referred to as nandopsines, caquetaines and amphilophines, and the Northern Central American Clade, including astatheroines, tomocichlines and herichthyines. Some of these groups have been previously identified, but often with different taxonomic compositions. Further resolution of Neotropical cichlid relationships, especially within the large amphilophine clade of Heroini, will require additional phylogenetic analysis. Nevertheless, the topology from this study provides a robust phyloge- netic framework for studying evolutionary diversification in Neotropical cichlids. Significantly-short branches at the base of Geophagini and Heroini are compatible with early bursts of divergence that are characteristic of adaptive radiations. This pattern suggests diversification of Neotropical cichlid gen- era occurred rapidly, with subsequent convergent, adaptive ecomorphological diversification among and within South and Central American clades. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction * Corresponding author. Address: Department of Natural History, Royal Ontario The rivers of South and Central America harbor the most diverse Museum, 100 Queen’s Park, Toronto, Ontario, Canada M5S 2C6. Fax: +1 416 586 freshwater fish fauna on Earth, with some estimates exceeding 5553. 6000 species, perhaps representing about 20% of all fishe and E-mail addresses: [email protected], [email protected] (H. López- Fernández), [email protected] (K.O. Winemiller), rodney.honeycutt@pepper- 10% of all species of vertebrates (Reis et al., 2003). Nearly 600 of dine.edu (R.L. Honeycutt). these species are cichlids, making the family the third most diverse 1055-7903/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2010.02.020 H. López-Fernández et al. / Molecular Phylogenetics and Evolution 55 (2010) 1070–1086 1071 in the Neotropics after Characidae and Loricariidae (Reis et al., on a multilocus phylogeny, López-Fernández et al. (2005a) pro- 2003). Neotropical cichlids (Cichlinae) are a monophyletic clade posed that the remarkable morphological, ecological and behav- that is sister to a monophyletic African cichlid clade (Pseudocre- ioral diversity of Geophagini genera was the outcome of an nilabrinae, Stiassny, 1991; Farias et al., 2000; Sparks and Smith, adaptive radiation, older than but similar to that seen for African 2004), and are found in nearly all rivers of South and Central Amer- lacustrine cichlids. Despite only partial success in resolving the ica, with species extending from the edge of Patagonia to Texas. geophagine phylogeny, López-Fernández et al.’s (2005a) work The Neotropical clade includes approximately 60 genera with showed that detailed taxon sampling and multiple datasets are many species still undescribed (Reis et al., 2003, HLF pers. obs.). important for both phylogenetic resolution and in-depth investiga- The great majority of Neotropical cichlid diversity has been classi- tion of speciation within the highly diverse Neotropical cichlid fied into three major tribes (Kullander, 1998; Smith et al., 2008): assemblage. Therefore, lack of a solid phylogeny limits taxonomic, Geophagini, Cichlasomatini and Heroini, with a handful of addi- ecological and evolutionary research. tional species placed in the tribes Cichlini, Retroculini, Chaetobran- A relatively stable taxonomy of South American cichlids has re- chini and Astronotini. Geophagini is restricted to South America sulted largely from the work of Kullander, who over a period of and southern Panama and includes approximately 18 genera and approximately three decades has revised nearly every South Amer- about 250 species (López-Fernández et al., 2005a,b). Cichlasoma- ican group and proposed the first classification of the Cichlinae tini includes 11 described genera and more than 70 species distrib- (e.g. Kullander, 1980, 1983, 1986, 1988, 1989, 1990, 1996, 1998; uted in South America and Panama. Heroini includes Kullander and Nijssen, 1989; Kullander and Silfvergrip, 1991). Kul- approximately 30 genera and about 150 spp. distributed in South lander’s (1983) revision of the genus Cichlasoma, which restricted and Central America, with one genus in Cuba and Hispaniola. the genus to twelve South American species, ‘‘orphaned” many Remarkably, little is known about the origin of Neotropical cich- species that were left without formal generic assignment. This lid diversity, as most studies of cichlid evolutionary diversification decision resulted in a series of studies describing a number of have focused on the unique adaptive radiations associated with the new genera of South American Cichlasomatini and Heroini and East African lakes Victoria, Tanganyika and Malawi (e.g. Meyer, revisions within Geophagini (e.g. Kullander, 1986, 1988, 1990; Kul- 1993; Kornfield and Smith, 2000; Streelman and Danley, 2003; Ko- lander and Nijssen, 1989), producing a more stable and tractable cher, 2004). In contrast to the Late Neogene-Quaternary origin of classification for South American cichlids. Unfortunately, the same African-lake cichlids (<7 Ma, e.g. Verheyen et al., 2003; Joyce has not been the case for the Central American Heroini, the taxon- et al., 2005), Neotropical cichlids have a long history of diversifica- omy of which has remained in a constant state of confusion and tion that appears to go back to the Late Cretaceous (>90 Ma, e.g. flux. Chakrabarty, 2006; López-Fernández and Albert, in press; Lund- In the absence of clear generic definitions for the Central Amer- berg et al., 2010). Consequently, Neotropical cichlid phylogenies ican cichlids previously included in Cichlasoma sensu lato, Central should be more tractable than those of the African-lake radiations American taxonomy requires major revision, but such revision (e.g. Farias et al., 2000; López-Fernández et al., 2005a,b; Concheiro has proven slow and difficult and is far from complete. Kullander Pérez et al., 2006; Rican et al., 2008; Musilová et al., 2009). Despite (1983) and Stiassny (1991) suggested that, until a clear phyloge- increasing interest in their evolutionary history, a fairly large num- netic understanding and diagnostic characters for the genera were ber of studies addressing aspects of their phylogeny, and a recent available, most orphaned species of the former Cichlasoma should claim to have solved their inter-generic relationships (Smith be designated