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Phylogenetic Relationships of African Killifishes in the Genera Aphyosemion and Fundulopanchax Inferred from Mitochondrial DNA Sequences William J

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Phylogenetic Relationships of African Killifishes in the Genera Aphyosemion and Fundulopanchax Inferred from Mitochondrial DNA Sequences William J Molecular Phylogenetics and Evolution Vol. 11, No. 3, April, pp. 351–360, 1999 Article ID mpev.1998.0566, available online at http://www.idealibrary.com on Phylogenetic Relationships of African Killifishes in the Genera Aphyosemion and Fundulopanchax Inferred from Mitochondrial DNA Sequences William J. Murphy1 and Glen E. Collier Department of Biological Sciences, The University of Tulsa, 600 S. College Avenue, Tulsa, Oklahoma 74104 Received May 12, 1997; revised June 17, 1998 Fundulopanchax, and Nothobranchius) and six mono- We have analyzed the phylogenetic relationships of typic genera (Adamus, Foerschichthys, Fundulosoma, 52 species representing all defined species groups (J. J. Pronothobranchius, Aphyoplatys, and Episemion). The Scheel, 1990, Atlas of Killifishes of the Old World, 448 composition and relationships of these genera have under- pp.) of the African aplocheiloid fish genera Aphyo- gone numerous changes as our knowledge of these fishes semion and Fundulopanchax in order to examine their has grown. The greatest number of changes have occurred interrelationships and to reveal trends of karyotypic with regard to the genus Aphyosemion Myers 1924. evolution. The data set comprised 785 total nucleotides The genus Aphyosemion was originally divided into from the mitochondrial 12S rRNA and cytochrome b genes. The molecular-based topologies analyzed by three subgenera: Aphyosemion, Fundulopanchax, and both maximum parsimony and neighbor-joining sup- Adinops. Those species assigned to Adinops were from port the monophyly of most previously defined species east Africa and were later removed to the genus groups within these two killifish genera. The genus Nothobranchius. The remaining species and subse- Aphyosemion is monophyletic except for the nested quent taxa assigned to these subgenera could be di- position of Fundulopanchax kunzi (batesi group; sub- vided by distributional criteria and independently by genus Raddaella) within this clade, suggesting that phenotypic criteria. The vast majority of these fishes this taxon was improperly assigned to Fundulopan- are found in small streams in the understory of the chax. The remaining Fundulopanchax species sampled rainforest (Scheel, 1990). The rainforest of equitorial were supported as being monophyletic in most analy- Africa is cleanly divided into western and eastern ses. Relationships among the species groups in both blocks by the Dahomey Gap, a strip of savanna habitat genera were not as strongly supported, suggesting that that extends to the coast in Benin, Togo, and eastern further data will be required to resolve these relation- Ghana. In 1966, Clausen recognized the distinctiveness ships. Additional sampling from the 16S rRNA gene allowed further resolution of relationships within Fun- of those species west of the Dahomey Gap. Subsequent dulopanchax, more specifically identifying the nonan- workers have identified additional morphological char- nual scheeli group as the basal lineage of this other- acters that distinguish these western taxa (Zee and wise annual genus. Chromosomal evolution within Wildekamp, 1995) and recent DNA sequence data Aphyosemion has been episodic, with the evolution of a (Murphy, 1997, Murphy and Collier, 1997, 1999) clearly metacentric complement having identify the western forms as a distinct clade not 10–9 ؍ reduced n occurred in multiple, independent lineages. Polarity of closely related to the eastern taxa. Thus the remaining chromosomal reductions within the elegans species problem with the genus Aphyosemion involves those group appears to support previous hypotheses concern- eastern species formerly assigned to the subgenera ing mechanisms of karyotypic change within the genus Aphyosemion and Fundulopanchax. Aphyosemion. ௠ 1999 Academic Press The subgenus Fundulopanchax was elevated to ge- neric level by Parenti (1981) based on two characters. Zee and Wildekamp (1995) dispute the diagnostic value INTRODUCTION of one of these characters but added four new charac- ters defining Fundulopanchax. Prominent among the African aplocheiloid killifishes are currently as- life history traits that distinguish Aphyosemion and signed to four speciose genera (Aphyosemion, Epiplatys, Fundulopanchax is annualism. Annual fishes (Myers 1942, 1955) are those that deposit their eggs in the 1 Present address: Laboratory of Genomic Diversity, National substrate where they withstand the dessication of an Cancer Institute, FCRDC, Frederick, MD 21702. annual dry season to hatch once the rains resume. 351 1055-7903/99 $30.00 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. 352 MURPHY AND COLLIER Members of Fundulopanchax are believed to be annual TABLE 1 while members of Aphyosemion are not (Parenti, 1981; Wildekamp, 1993). Taxa Under Study, Proposed Species Groups and Their Abbreviations Used in Figures (Scheel, 1990), and Chromosome complements are relatively well con- Various Subgeneric Names Assigned to Specific Taxa served in teleostean fishes, particularly within the immense acanthomorph clade (sensu Johnson and Pat- Species group1/ terson, 1993) in which the predominant diploid karyo- species sampled Subgenus type is 2n ϭ 48 (Sola et al., 1981). Significant deviations Genus Aphyosemion from this number have occurred in only a handful of bivittatum group (BIV) Chromaphyosemion2 these fish species. One order in particular, the Cypri- bivittatum,* volcanum, sp. LEC 93/27 nodontiformes (killifishes), displays a striking propen- calliurum group (CAL) Mesoaphyosemion3 sity for clade-specific karyotypic rearrangement. Per- ahli, australe,* calliurum, celiae haps the best example is the aplocheiloid genus cameronense group (CAM) Mesoaphyosemion cameronense, maculatum, mimbon Aphyosemion, which shows more inter- and intraspe- coeleste group (COL) Mesoaphyosemion cific chromosomal rearrangements (Scheel, 1990) than aureum, citrinepinnis, coeleste, occe- perhaps any other fish genus. Our knowledge of the latum types of mechanisms behind karyotypic evolution, and elegans group (ELE) Mesoaphyosemion christyi, cognatum (2), decorsei, elegans its potential contribution to speciation within this (3), lamberti, melanopteron, punc- genus, have been hampered by the lack of a phyloge- tatum, rectogoense, wildekampi netic framework for this diverse group. exiguum group (EXI) Kathetys4 The specific aim of this work was to use mitochon- bualanum, exiguum 5 drial DNA sequences to assess the monophyly and georgiae group (GEO) Diapteron cyanostictum composition of Aphyosemion and Fundulopanchax, to striatum group (STR) Mesoaphyosemion determine the monophyly of recently proposed subgen- exigoideum, gabunense, louessense, era and species groups (Scheel, 1990; Table 1) within ogoense, primigenium, striatum these genera, and to determine the polarity of chromo- ungrouped (UG) somal rearrangements within the molecular phylogeny. labarrei Mesoaphyosemion? Genus Fundulopanchax Further, this enlarged data set has allowed further arnoldi group (ARN) Paludopanchax6 consideration of the origin of annualism (Murphy and filamentosum, robertsoni, walkeri Collier, 1997) within these genera. We sampled 36 batesi group (BAT) Raddaella7 populations of 32 described and 4 undescribed species kunzi 8 of Aphyosemion and 16 species of Fundulopanchax. In gardneri group (GAR) Paraphyosemion cinnamomeum, gardneri, mirabile* total these represent 14 of Scheel’s (1990) 15 species gulare group (GUL) Gularopanchax9 groups. The 15th group, composed of a single species, deltaense, fallax, gulare, schwoiseri, Pronothobranchius kiyawensis, has been subsequently sjoestedi* excluded from Aphyosemion on the basis of both morpho- ndianum group (NDI) Paraphyosemion10 amieti, ndianum logical and molecular characters (Parenti, 1981; Mur- scheeli group (SCE) Paraphyosemion8 phy, 1997). santaisabellae, scheeli Note. Generic divisions follow those of Parenti (1981). Numbers in MATERIALS AND METHODS parentheses denote number of populations sampled. Data from taxa marked with asterisks have previously been reported (Murphy and A list of the taxa examined and their sources is in the Collier, 1997). Appendix. Mitochondrial DNA was extracted from 1 Scheel, 1990. muscle or liver tissues. Mitochondrial DNA extractions 2 Radda, 1971. 3,6,9,10 Radda, 1977. and amplification protocols were performed as previ- 4,7 Huber, 1977. ously described (Murphy and Collier, 1996). Some of the 5 Huber and Seegers, 1977. sequences have been previously reported (see Table 1). 8 Kottelat, 1976. We sequenced a 360-bp region of the cytochrome b (cytb) gene and a 425-bp region of the 12S rRNA gene. The primers used were L14724 and H15149 (Kocher et products were purified with 30,000 MW regenerated al., 1989; Meyer et al., 1990) for the cytb segment and cellulose filter devices (Millipore Inc.). Cycle sequenc- L1091 and H1478 (Kocher et al., 1989) for the 12S ing using fluorescent-labeled terminators was per- rRNA segment. Primers 16Sar-L and 16Sbr-H (Palumbi formed using Ampli-Taq FS DNA polymerase (Applied et al., 1991) were used to amplify a region of the 16S Biosystems Inc.). The reactions were purified free of rRNA gene for Fundulopanchax taxa. The new DNA fluorescent terminators using Centri-Sep columns sequences were generated with an automated se- (Princeton Separations) before loading onto a sequenc- quencer (ABI 373 Stretch). Symmetric amplification ing gel (6% Long-Ranger acrylamide, FMC). PHYLOGENETIC RELATIONSHIPS OF AFRICAN KILLIFISHES 353 Sequences were initially aligned using the program AF002401. The total analyzed data
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