The Family Alestidae (Ostariophysi, Characiformes): a Phylogenetic Analysis of a Trans-Atlantic Clade

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The Family Alestidae (Ostariophysi, Characiformes): a Phylogenetic Analysis of a Trans-Atlantic Clade Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2005? 2005 145? 1144 Original Article PHYLOGENETIC RELATIONSHIPS OF ALESTIDAEA. M. ZANATA and R. P. VARI Zoological Journal of the Linnean Society, 2005, 145, 1–144. With 44 figures The family Alestidae (Ostariophysi, Characiformes): a phylogenetic analysis of a trans-Atlantic clade ANGELA M. ZANATA1 and RICHARD P. VARI FLS2* 1Departamento de Zoologia, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Geremoabo, Ondina, Salvador, BA 40170-290, Brazil 2Department of Vertebrate Zoology, MRC-159, National Museum of Natural History, PO Box 37012, Smithsonian Institution, Washington, DC 20013-7012, USA Received September 2004; accepted for publication March 2005 The overall most parsimonious hypothesis of relationships based on 200 characters indicates that the Alestidae is the closest relative of Chalceus, a genus previously assigned to the Neotropical Characidae. Chalceus is shifted into the Alestidae, which becomes the only trans-Atlantic family level group within the Characiformes. Various previously proposed suprageneric assemblages within the Alestidae (e.g. Petersiini) failed to delimit monophyletic groups under the intrafamilial phylogenetic analysis. The evaluation of fossil alestids within the context of the phylogeny indicates that the ancestors of Alestes, Arnoldichthys, Brycinus, Bryconaethiops and Hydrocynus evolved prior to the early Eocene (Cuisian of Upper Ypresian), 49–54.8 million years ago, with the fossil Alestoides most closely related to Alestes. The phylogenetic information further indicates a minimum age of 90–112 million years for the Alestidae. Contrary to previous hypotheses, the fossil African Sindacharax was found to be most similar to the clade including the alestid genus Bryconaethiops rather than most closely related to the South American subfamily Serrasalminae. Evaluation of the fossil Mahengecharax carrolli fails to support its hypothesized placement as the sister group to all Recent members of the Alestidae. Two separate episodes of miniaturization and one episode of gigantism occurred within the evolution of the Alestidae. © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 1-144. No claim to original US government works. ADDITIONAL KEYWORDS: African Characidae – Chalceus – fossil evidence – gigantism – miniaturization – phylogeny – Sindacharax. INTRODUCTION tidae and Citharinidae (Vari, 1979); a clade formed by the putatively monotypic family Hepsetidae; and the The Characiformes, one of the major lineages of ostar- assemblage recognized alternatively as the ‘African iophysan fishes, is widely distributed through fresh- Characidae’, Alestinae, or Alestidae by previous waters of major portions of the Americas and Africa. authors and hereafter referred to as the Alestidae. New World characiforms occur from the southern These studies have revealed that the three African boundary regions of the United States to the central subunits of the Characiformes do not jointly constitute portions of Chile and Argentina. Characiforms inhabit a monophyletic unit, being instead dispersed across freshwater ecosystems across broad regions of sub- the phylogeny of the order. That conclusion is inter- Saharan Africa with the exception of the southern por- esting both phylogenetically and in terms of the his- tions of the continent and the Horn of Africa, with the torical biogeographical relationships of the South ranges of several characiform species extending American and African freshwater fish faunas. through the Sahara Desert along the length of the Nile Both the monophyly and higher-level phylogenetic River basin. Phylogenetic studies in recent decades relationships of the clade consisting of the Disticho- have delimited three subunits among African characi- dontidae and Citharinidae have been the subject of forms: a clade consisting of the families Distichodon- in-depth analyses using morphological (Vari, 1979; Fink & Fink, 1981) and molecular (Ortí, 1997; Ortí & *Corresponding author. E-mail: [email protected] Meyer, 1997) evidence that consistently supports the © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 1–144 No claim to original US government works 1 2 A. M. ZANATA and R. P. VARI hypothesis of the monophyly of the clade and/or its The phylogenetic position of, and intrarelationships basal position within the Characiformes. Hypotheses within, the African characiforms that constitute nearly as to the phylogenetic relationships of the Hepsetidae all of the Alestidae of this study are yet to be examined (Vari, 1995; Buckup, 1998; Oyakawa, 1998) align that in depth. Greenwood et al. (1966: 395) united the spe- family with the New World families Ctenoluciidae, cies now assigned to the Alestidae together with a Erythrinidae and Lebiasinidae, albeit with these large number of New World taxa into the Characidae. hypotheses advancing alternative patterns of relation- That family constituted the most speciose assemblage ships among the four families. Preliminary informa- within the Characiformes (the Characoidei of Green- tion also indicates that the Hepsetidae can be defined wood et al., 1966). This expansive Characidae, a con- on the basis of several derived attributes (Vari, 1995: cept that has been retained by some authors until the 37). present time (Lévêque, 2001: 14), was, furthermore, The Alestidae (African members of the Characidae the only characiform family common to the Americas of Greenwood et al., 1966), the third group among and Africa. A series of phylogenetic analyses (Buckup, African characiforms, occurs across the range of the 1998; Lucena & Menezes, 1998; Toledo-Piza, 2000; this order in Africa. Maximum diversity in the Alestidae, study) demonstrated that such a broadly encompass- both in numbers of genera and species, occurs in the ing Characidae constituted a nonmonophyletic group coastal rivers of West Africa and the Congo River within the Characiformes. basin. Correlated with increasing distances from those Of particular note for the present study was the regions is a decreasing diversity of alestids at both the hypothesis that the African members of the Chara- generic and specific taxonomic levels. The approxi- cidae (sensu Greenwood et al., 1966) constituted the mately 105 species in the Alestidae (Paugy, 1984, sister group to a clade that encompassed more than 1986; Teugels & Thys van den Audenaerde, 1990; just the Neotropical components of the Characidae. Géry, 1995, 1996) range from the diminutive species of Several phylogenetic studies focusing on these compo- the West African genus Virilia, some of which mature nents, including some alestids in the outgroup analy- at 18.8 mm standard length, to the tigerfish, Hydro- sis, suggested a close relationship between the cynus goliath which at 1320 mm standard length Alestidae and at least some components of the Chara- achieves the greatest length of any characiform cidae (Ortí & Meyer, 1997; Buckup, 1998; Zanata, (Weitzman & Vari, 1998). Such a dramatic range in 2000) and provided preliminary evidence for the body size, 18.8–1320 mm, a 70¥ size range, is unique monophyly of the Alestidae (Vari, 1998: 120; Zanata, to members of the Alestidae among the families of the 2000: 293). Some of these analyses, however, raised Characiformes hypothesized to be monophyletic on questions as to the monophyly of a group consisting of the basis of multiple synapomorphies. the New World Characidae and the African Alestidae. Although Buckup (1998: 139) remarked that the Of particular note relative to that question are the monophyly of the Alestidae ‘has never been disputed’, striking similarities between the monotypic African a retrospective evaluation indicates that this assump- genus Arnoldichthys that was assigned to the Ales- tion is predicated on a lack of evidence indicative of tidae by recent authors and the South American the nonmonophyly of the Alestidae rather than being characid genus Chalceus, a lineage of five mid-sized derived from a robust phylogenetic analysis that species (Zanata & Toledo-Piza, 2004). So pronounced yielded a series of hypothesized synapomorphies for are the similarities between these two genera that a the family. Previous phylogenetic studies that delved species of Chalceus with erroneous locality data was into the question of the monophyly of the Alestidae did described as a new genus and species of a supposedly so in passing and the resultant hypotheses of alestid African characid (= alestid) by Fowler (1906). In a monophyly were invariably incidental to phylogenetic study focused on the question of the phylogenetic rela- analyses focused on other groups within the Characi- tionships within the Neotropical characid genus formes (Vari, 1998: 120). All such hypotheses on the Brycon, Zanata (2000) identified characters that sup- monophyly for the Alestidae were, furthermore, based ported the hypothesis of a close relationship of Chal- on evidence derived from the sampling of a typically ceus with some genera of the Alestidae. An in-depth very limited subset of taxa in the Alestidae. In their analysis of that hypothesized phylogenetic relation- recent publication focused on the question of the rela- ship lay, however, beyond the limits of her study. tionships of Alestes and Brycinus, Murray & Stewart Intrafamilial suprageneric and generic groupings (2002) proposed a series of synapomorphies for the within the Alestidae
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