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Molecular Insights Into the Phylogeny of Mormyriform Fishes and The Original Paper Brain, Behavior and Evolution Brain Behav Evol1997;49:324-351 Jose Alves-Gomes•""" Carl D. Hopkinsc,d Molecular Insights into the ' Instituto Nacional de Pesquisas da Phylogeny of Mormyriform Fishes Amazonia, Manaus, Brazil; b Scripps Institution of Oceanography, University of California, San Diego, and the Evolution of Their La Jolla, Calif., USA; ' Section of Neurobiology and Behavior, Cornell University, Ithaca, N.Y., USA; Electric Organs d Centre International de Recherches Medicales Franceville, Franceville, and Institut de Recherche en Ecologie Tropicale, Makokou, Gabon Key Words Abstract Mormyriformes In this report we generate a partial' phylogeny of the mormyriform fishes using Molecular phylogeny mitochondrial DNA sequences from twelve species of mormyriforms belonging Electrocyte designs to five genera. Electric organs and electric organ discharges are also examined. Electric organ evolution We have sequenced and aligned 373 bases from the mitochondrial 12S rRNA Electric fish and 559 bases from the 16s rRNA from fourteen species of the superorder Os­ EOD teoglossomorpha. Two non-mormyriform genera were used as outgroups. Three phylogenetic methods generated concordant partial phylogenies for these fish. Our analysis focuses on the genus Brienomyrus, which is a heterogeneous clade with at least eleven nominal species. Six morphs from Gabon had distinctive EODs but were morphologically 'cryptic' in that they all had the brachyistius­ like body morphology. DNA analysis fully supports the EOD data that the six morphs represent distinct clades. The group from Gabon is monophyletic, while B. brachyistius from West Africa is a separate lineage. B. niger, a second distinct lineage, is a sister group to the six species from Gabon. Petrocephalus is the sis­ ter group of all the genera of the subfamily Mormyrinae so far analyzed, thereby confirming previous osteological results. Gymnarchus niloticus is the sister group of the family Mormyridae, also confirming an earlier phylogenetic hypo­ thesis based on morphology. The molecular data adds polarity to electric organ characteristics. Stalkless electrocytes appear to be primitive. Petrocephalus, with non-penetrating stalked electrocytes innervated on the posterior side,represents an ancestral state for the Mormyridae, while Marcusenius, Brienomyrus and Gnathonemus with penetrating-stalked electrocytes, represent the apomorphic condition. Two species with doubly-penetrating electrocytes innervated on the posterior side may represent a transitional stage. At least two species of Brieno­ myrus appear to have reverted to non-penetrating stalked electrocytes, possibly through paedomorphosis. © 1997 S. Karger AG, Basel Jose Alves-Gomes KARGER Section of Neurobiology and Behavior E-Mail [email protected] Cornell University FaX+41 61 306 12 34 This article is also accessible online at: Ithaca, NY 14853 (USA) http://www.karger.ch http://BioMedNet.com/karger Introduction thought to be related to Brienomyrus brachyistius [Gill, 1862], were given temporary names such as B. brachyis­ With about 200 nominal species, the mormyriform elec­ tius 'biphasic' (bp), B. brachyistius 'long biphasic' (lbp), tric fishes (order Mormyriformes, Osteoglossomorpha) B. brachyistius 'triphasic' (tp) and B. brachyistius 'mono­ comprise one of the most diverse clades of freshwater phasic' (mp) [Hopkins, 1980; Hopkins and Bass, 1981; Bass fishes from Africa and the largest group of electric fishes and Hopkins, 1983; Bass, 1986a; Basset al., 1986]. Since the known. The mormyriforms have been the subject of wide­ electric discharges in these mormyriforms are used for so­ spread neurobiological interest ever since Lissmann [1951] cial communication and play a vital role in species recogni­ discovered that they produce weak electric discharges. tion [Hopkins and Bass, 1981; Hopkins, 1986], these EOD They have been used in behavioral, electrophysiological, types appear to define distinct clades which are repro­ anatomical, and developmental studies of the electric or­ ductively isolated. Three of these species are undescribed, gans, e1ectroreceptors, and the central nervous system, but while one (identified as B. brachyistius monophasic by little is known about their phylogenetic history. Most of the Hopkins [ 1980]) has been reidentified as Brienomyrus systematic work, based on traditional analyses of morpho­ batesii [based on Boulenger, 1906]. Recent studies have logical characters, has not included phylogenetic or cladis­ revealed morphological, behavioral, and ecological differ­ tic reasoning [Orts, 1967; Taverne, 1972; Daget et al., 1984]. ences between the EOD-types that confirm the spe­ According to Taverne [1972] and Gosse [1984] there are 199 cies-level status of these groups; species descriptions are nominal species of mormyriforms belonging to 18 genera. currently underway. In the past, without EODs, authors Taverne considers the order Mormyriformes to be com­ may have confused these species with other forms [see posed of the families Gymnarchidae and Mormyridae. Trewavas, 1974; Bigorne 1990]. While the Gymnarchidae has a single species, Gymnarchus Taverne designated Brienomyrus brachyistius [Gill, niloticus, the family Mormyridae is composed of two sub­ 1862] as the type species for Brienomyrus. He also listed families: the Petrocephalinae (26 species) and the Mormy­ five other species for the genus: B. niger [GUnther, 1866]; rinae (165 species). Since Taverne's work there have been B. sphecodes [Sauvage, 1878]; B. longianalis [Boulenger, several new species added to the group [Gosse, 1984], a 1901]; B. adustus [Fowler, 1936], and B. jacksoni [Poll, number of revisions of genera based on regional data 1967]. Taverne [1972] also defined two sub-genera, Brieno­ [Leveque et al., 1990], and a number of studies of compar­ myrus (Brienomyrus) and Brienomyrus (Brevimyrus ), plac­ ative biology of the group [Hopkins and Bass, 1981; Bass, ing Brienomyrus (Brevimyrus) niger into one sub-genus 1986a, 1986b]. and the remainder into Brienomyrus (Brienomyrus). Since With the recent interest in the neurobiology and behav­ then, B. jacksoni was put into the genus Paramormyrops, ior of electric fish there is good reason to examine the phy­ and four new species were added to Brienomyrus (Brie­ logeny of this group using alternative data sets such as mo­ nomyrus): B. curvifrons [Taverne, 1977]; B. longicaudatus lecular information. In this paper we attempt a preliminary [Taverne, 1977]: B. hopkinsi [Taverne and Thys van den phylogenetic analysis of several subgroups of mormyri­ Audenaerde, 1985], and B. tavernei [Poll, 1972]. Bigorne forms using mitochondrial DNA sequences. [ 1989] provided a revision of the Brienomyrus of West Africa and added B. batesii [Boulenger, 1906] (formerly Genus Brienomyrus Hippopotamyrus) to the genus. Mamonekene and Teugels This paper will focus on the genus Brienomyrus (for­ [1993] added B. kingsleyae [GUnther, 1896] (formerly Pol­ merly Marcusenius), a morphologically heterogeneous limyrus). clade with eleven known species. The genus Brienomyrus In addition to the difficulty of identifying some of the was established in 1971 by Taverne [1971a], but the litera­ Brienomyrus in museum speciemens without the benefit of ture on this genus has been particularly confusing, espe­ the EODs, confusion over Brienomyrus from Central cially for fish from the forests of Central West Africa where Africa is in part due to confused synonomies for Brieno­ one finds the greatest number of species. In previous pub­ myrus brachyistius. The list includes Mormyrus micro­ lications on the mormyrids of Gabon, Hopkins and col­ cephalus [GUnther, 1867] with a type locality in the Ogooue leagues have shown that it is possible to identify live River in Gabon; Marcusenius longianalis [Boulenger, 1901] Brienomyrus on the basis of electric organ discharge (EOD) from the Niger Delta, and Marcusenius adustus [Fowler, characteristics [Hopkins, 1981, Bass et al., 1986; Hopkins 1936] from Cameroon [Trewavas, 1974]. Molecular phylo­ and Westby, 1986; Friedman and Hopkins, 1996]. Four mor­ genies, in conjunction with morphological and behavioral phologically similar species with distinguishable EODs, data can help us to understand the evolutionary relation- Molecular Phylogeny and Brain Behav Evol 1997;49:324-351 325 Mormyriform Bioelectrogenesis ships among these confusing groups. This study sheds light peatedly fuse with others, increasing in diameter until they on the relationships among morphologically similar reach a large trunk where they receive synaptic input from Brienomyrus clades from Gabon using molecular methods. electromotor nerve axons. This entire root system is called a 'stalk' [Bennett and Grundfest, 1961; Bennett, 1971] or a Mitochondrial DNA (mtDNA) 'pedicule' [Szabo, 1960, 1961]. In this study we use mtDNA sequences to estimate phy­ We recognize four principal types of electric organs logenetic relationships. There is presently extensive in­ among the mormyriforms we sampled (fig. 3). Our obser­ formation available about the mitochondrial genome of vations support and extend the observations of Ogneff several vertebrate and invertebrate orders. In particular, [1898], Schlichter [1906], Gosse and Szabo [1960], Bennett ribosomal RNA genes have been shown to be suitable for and Grundfest [1961], Bennett [1971] and Bass [1968a], who phylogenetic studies addressing inter-specific as well as recognized a number of other variations in morphology. inter-familial realtionships. Among vertebrates,
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