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Brieno Cytb Formatted.Doc Left © John P. Sullivan Revision Date: November 16, 2000 70 pages 8972 Words 1 table, 7 figures File: brieno cytb formatted.doc Left running head: Sullivan, Lavoue and Hopkins Right running head: Analysis of a riverine species flock DISCOVERY AND PHYLOGENETIC ANALYSIS OF A RIVERINE SPECIES FLOCK OF AFRICAN ELECTRIC FISHES (MORMYRIDAE: TELEOSTEI) by John P. Sullivan1,3, Sébastien Lavoué2, Carl D. Hopkins1 1Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, USA 14853. 2Museum National d’Histoire Naturelle, Ichtyologie Générale et Appliquée; 43 rue Cuvier 75005, Paris, France. 3Department of Ichthyology, American Museum of Natural History, Central Park West at 79th St, New York, NY, USA 10024. Correspondence to: Carl D. Hopkins [email protected] phone: 1-607-255-2259 fax: 1-607-254-4308 Keywords: electric fish, species flock, speciation, cytochrome b, phylogeny Sullivan, Lavoué and Hopkins Analysis of a riverine species flock ABSTRACT We have discovered surprising undescribed diversity within a clade of mormyrid electric fish in our recent collections from the Ogooué and Ntem River basins of Gabon, Africa. We recognize 38 distinct forms within this group on the basis of unique morphologies and electric organ discharge (EOD) characteristics of which only four clearly correspond to described species. The remaining 34, treated here as operational taxonomic units (OTUs), may represent as many new species. We sequenced the complete cytochrome b gene from 86 specimens sampled from these OTUs and recovered 65 distinct cytochrome b haplotypes. Trees obtained by both maximum parsimony and maximum likelihood analyses, rooted with sequence data from outgroup taxa, provide strong support for the monophyly of all 38 of these OTUs. The small genetic distances between many distinct forms suggests an ongoing and rapid radiation. However, in many instances, the cytochrome b tree topology fails to support the monophyly of individual OTUs or close relationships between OTUs which are similar in morphology and EOD characteristics. In other cases, individuals from distinct 1 Sullivan, Lavoué and Hopkins Analysis of a riverine species flock OTUs share identical, or nearly identical, haplotypes. We infer from these results a disjunction between the mitochondrial gene tree and the overall species phylogeny of these organisms. The presence of divergent haplotypes within single populations of some forms suggests incomplete mitochondrial lineage sorting, while the grouping of phenotypically distinct, but geographically proximate forms in other cases suggests local hybridization and introgression of mitochondrial genomes among forms. Both incomplete lineage sorting and introgression may contribute to the lack of congruence between the mitochondrial gene tree and the natural groups supported by morphological and EOD data. Diversification in this clade of riverine electric fishes and the problems associated with recovering a meaningful species-level phylogeny from mitochondrial data suggest a parallel to the well-known lacustrine fish “species flocks.” Social selection on EOD waveforms may be involved in the rapid radiation of these fishes. 2 Sullivan, Lavoué and Hopkins Analysis of a riverine species flock INTRODUCTION The African weakly electric fish superfamily Mormyroidea (families Mormyridae + Gymnarchidae) represents a remarkable modern radiation from within the Superorder Osteoglossomorpha: one of the oldest and phylogenetically most basal groups of extant teleosts (Arratia 1997; Greenwood 1973; Lauder and Liem 1983; Patterson and Rosen 1977). This radiation in African freshwater riverine environments has occurred while, according to the fossil record, other osteoglossomorph lineages have undergone substantial reduction in their global diversity and distribution since the Early Tertiary (Li 1997). Over 200 species of mormyroids in 19 genera are recognized (Daget et al. 1984). In comparison, the remaining living osteoglossomorphs, although distributed on all continents except Europe and Antarctica, comprise only 18 species in 10 genera (Nelson 1994). Uniquely among the osteoglossomorphs and undoubtedly related to their evolutionary success, all mormyroids electrolocate and communicate by means of specialized electric organs and electroreceptors. In this paper we present evidence based on recent collections in Gabon in West Central Africa that this 3 Sullivan, Lavoué and Hopkins Analysis of a riverine species flock radiation is ongoing explosively in at least one group of mormyroids. Within this group we have identified many taxonomically unrecognized forms possessing distinct electric organ discharge (EOD) waveforms and morphological characteristics. Based on the overall similarity of these characteristics we have sorted the specimens into operational taxonomic units (OTUs) and have investigated their phylogenetic relationships by analysis of sequence data from the mitochondrial cytochrome b gene. Our goals were to establish (1) whether morphological, EOD and molecular data would provide congruent definitions of OTUs and higher-level natural groups within this clade of fishes and (2), whether a molecular phylogeny of these entities would reveal patterns of EOD and electric organ evolution at the species level. Taxonomy and previous phylogenetic studies of the genera Brienomyrus and Paramormyrops The genus Brienomyrus was established by (Taverne 1971) as part of his taxonomic revision of the Mormyridae based upon osteology, but without explicit reference to any uniquely shared derived characters (synapomorphies). Within the genus, he recognized two subgenera: B.(Brienomyrus) and B.(Brevimyrus). Currently, there are 4 Sullivan, Lavoué and Hopkins Analysis of a riverine species flock nine valid species within the first subgenus (B. brachyistius, B. longianalis, B. sphekodes, B. kingsleyae, B. curvifrons, B. longicaudatus, B. batesii, B. taverni, and B. hopkinsi) and a single species (B. niger) in the latter (Alves-Gomes and Hopkins 1997; Teugels and Hopkins 1998). The genus Paramormyrops was also established by Taverne (1977a) for the species Paramormyrops gabonensis from the Ivindo River of Gabon and to which he referred Marcusenius jacksoni Poll, from the Upper Zambesi basin of Angola. Taverne apparently did not include P. gabonensis within Brienomyrus due the presence of an ossified lateral ethmoid in this species, a character absent in the Brienomyrus that he examined. Recent studies have demonstrated the polyphyly of the genus Brienomyrus with several molecular datasets (Alves- Gomes and Hopkins 1997; Lavoué et al. 2000; Sullivan et al. 2000). Lavoué et al. (submitted) performed an unweighted parsimony analysis on the combined data used in these previous studies (from the mitochondrial 12S, 16S, cytochrome b and nuclear RAG2 genes) with new sequence data from two introns in the nuclear S7 gene for 38 species belonging to 17 nominal genera within the subfamily Mormyrinae. The single most parsimonius tree which results 5 Sullivan, Lavoué and Hopkins Analysis of a riverine species flock (Fig. 1) indicates that Brienomyrus (Brienomyrus) brachyistius, the type species of the genus, is the sister species not to any other included Brienomyrus species, but to Isichthys henryi. These species together form the sister group to included species of the genus Mormyrus. Quite separate from this clade, Brienomyrus (Brevimyrus) niger is weakly supported as the sister species to Hyperopisus bebe at the base of a large clade containing species of Marcusenius, Hippopotamyrus, Gnathonemus and Campyolomormyrus. A third clade containing nominal Brienomyrus species (B.hopkinsi, B. longicaudatus) in addition to Paramormyrops gabonensis and an undescribed species (= VAD in this study) appears as the sister group to Marcusenius conicephalus. These species (including M. conicephalus) are endemic to a particular region of Lower Guinea: the Ogooué, Ntem, and Woleu/Mbini River basins of Gabon, southern Cameroon and Equatorial Guinea. The sister group of these taxa is a clade containing taxa endemic to the same region: Boulengeromyrus knoepffleri, Ivindomyrus opdenboschi and Pollimyrus marchei (Daget et al. 1984; Kamdem Toham 1998). In addition to high bootsrap and decay index values in this analysis, the monophyly of this third clade of Brienomyrus species plus Paramormyrops gabonensis is supported by a 6 Sullivan, Lavoué and Hopkins Analysis of a riverine species flock unique 22 base pair inversion in the first intron of the S7 gene (Lavoué et al. submitted). It is this third, taxonomically unrecognized clade with which we are concerned in this study. Despite their demonstrated remote relationship to the type species of Brienomyrus and the inclusion of Paramormyrops gabonensis, we henceforth refer to them as the “Gabon-clade Brienomyrus.” We have begun morphological studies to search for non-molecular synapomorphies of this group and species descriptions and a revision of their taxonomy are underway. The Gabon-clade Brienomyrus Gabon-clade Brienomyrus species range in adult size from about 100 to about 250 mm standard length. They have moderately compressed bodies which are relatively elongate compared to most other mormyrids, rounded non-tubular snouts with small terminal to somewhat subterminal mouths bearing 5-9 (upper jaw) and 6-9 (lower jaw) bicuspid pincer-like teeth. They have fleshy, somewhat bulbous chins, small but functional eyes and are light gray or light brown to near black in color with little patterning of body pigmentation. They are nocturnally
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