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Phylogeny and Evolutionary Radiation in Seasonal Rachovine Killifishes: Biogeographical and Taxonomical Implications

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Phylogeny and Evolutionary Radiation in Seasonal Rachovine Killifishes: Biogeographical and Taxonomical Implications 64 (2): 177 – 192 © Senckenberg Gesellschaft für Naturforschung, 2014. 25.7.2014 Phylogeny and evolutionary radiation in seasonal rachovine killifishes: biogeographical and taxonomical implications Wilson J. E. M. Costa Laboratory of Systematics and Evolution of Teleost Fishes, Institute of Biology, Federal University of Rio de Janeiro, Caixa Postal 68049, CEP 21944-970, Rio de Janeiro, Brasil; wcosta(at)acd.ufrj.br Accepted 26.v.2014. Published online at www.senckenberg.de/vertebrate-zoology on 15.vii.2014. Abstract A phylogenetic analysis combining available mitochondrial DNA sequences (total of 3,339 bp) and 161 morphological characters for 22 species of rachovine genera (Aphyolebias, Austrofundulus, Gnatholebias, Llanolebias, Micromoema, Moema, Neofundulus, Pterolebias, Rachovia, Renova, Terranatos, and Trigonectes), and 16 outgroups, supports monophyly of the group containing genera endemic to the Orinoco river basin and adjacent coastal drainages. Results of the present analysis are compared to previous studies. The tree topology indicates that the genera Moema and Rachovia as presently delimited are paraphyletic; consequently, Aphyolebias and Austrofundulus are respectively placed in the synonymy of Moema and Rachovia. This study also indicates that rachovines were in the past geographically restricted to the Ama]onas3araguay area where diversi¿cation in niche e[ploitation was constrained by competition with sympatric mem- bers of older seasonal ¿sh lineages. Rachovines later reached the Orinoco basin and adjacent coastal drainages by dispersal through the Paleo-Amazonas river basin, when major evolutionary radiation taken place. Key words Amazon Forest, Amazonas river, Orinoco river, Phylogeny, Biogeography. Introduction Independent molecular phylogenies (HRBEK & LARSON, nomenclatural priority over other suprageneric names in- 1999; MURPHY et al., 1999) using mitochondrial DNA volving the group. (mt-DNA) sequences have corroborated a group of sea- The Rachovini, as herein delimited, was not recog- sonal killi¿shes, endemic to central and northern parts of nised in former phylogenetic analyses, which used only South America, including the present genera Aphyolebias a few informative morphological characters for species COSTA, 1998, Austrofundulus MYERS, 1932, Gnatholebias of this group (PARENTI, 1981; COSTA, 1990b, 1998). All COSTA, 1998, Llanolebias HRBEK & TAPHORN, 2008, Mi- species of this group are seasonal ¿shes, uniquely found cro moema COSTA, 1998, Moema COSTA, 1989, Neo fun- in temporary pools formed during the rainy seasons, a dulus MYERS, 1924, Pterolebias GARMAN, 1895, Ra cho- unique life style occurring both in American and African via MYERS, 1927, Renova THOMERSON & TAPHORN, 1995, aplocheiloid killi¿shes (e.g., PARENTI, 1981; COSTA, Terranatos TAPHORN & THOMERSON, 1978, and Tri go- 1998). As already noted by COSTA (1998), some mor- nectes MYERS, 1925. This group is herein referred as phological features have independently arisen in differ- tribe Rachovini, a name erected in COSTA (1990a) having ent seasonal ¿sh lineages, generating some ambiguity in ISSN 1864-5755 177 W.J.E.M. Costa: Phylogeny and evolutionary radiation in seasonal rachovine killifishes phylogenetic analyses. Consequently, some rachovines 1991), and Rivulus cylindraceus POEY, 1860. A com- were formerly considered to be more closely related to plete list of material e[amined appears in COSTA (2012). members of other seasonal ¿sh lineages than to most ra- Fragments of the following mt-DNA genes were ana- chovines, but subsequent morphological phylogenies di- lysed cytochrome b (cytb), cytochrome o[idase I (co[1), rected to part of rachovines (COSTA, 2005) or to another 12S ribosomal RNA (12S) and 16S ribosomal RNA (16s) rivulid clade (COSTA, 2011a) have reported characters po- ¿rst analysed by MURPHY et al. (1999), and, transfer tentially diagnostic for the tribe. On the other hand, mo- RNAs for valine, glutamine, methionine, tryptophan, lecular phylogenetic studies have indicated conÀicting alanine, asparagines, cysteine, and tyrosine, and NADH relationships among rachovine genera (HRBEK & LARSON, dehydrogenase subunit II (ND2), ¿rst analysed by HRBEK 1999; MURPHY et al., 1999). These studies used slightly & LARSON (1999); protocols for e[traction, ampli¿ca- different set of terminal ta[a and distinct gene samples tion and sequencing, tests for differential saturation, and of the mitochondrial genome. As a result of incongru- GenBank accession numbers are available in HRBEK & ent phylogenies, relationships among some rachovine LARSON (1999) and MURPHY et al. (1999). Sequences genera are still poorly understood. The primary objective were aligned using Clustal-W (CHENNA et al., 2003) and of the present study is to concatenate mt-DNA available subsequently optimized manually; regions of sequences in those studies in a single analysis, combining them to showing high degree of ambiguity for alignment, mak- morphological ta[a in order of to search the best phy- ing homology of sites questionable, were deleted from logenetic tree using a total evidence approach, which is the ¿nal aligned sequence, which had a total of 3,339 the basis for a discussion on evolutionary radiation and bp. Morphological characters were obtained from recent biogeography of rachovines. phylogenetic studies involving rachovines (COSTA, 1998, 2005, 2011a), besides new characters derived from the comparative analysis of brain morphology and osteologi- cal and myological structures. Morphological characters with a derived character state occurring in a single ter- Material and methods minal ta[on were e[cluded. The analysis includes a total of 161 characters, listed in Appendi[ 1, where charac- ter statements are formatted following SERENO (2007); complete descriptions of morphological traits will ap- Terminal ta[a were species with mt-DNA sequences avail- pear elsewhere (COSTA, in prep.) Osteological prepara- able in *enBank, including 22 rachovine in-group ta[a, tions (c&s) were made according to TAYLOR & VAN DYKE Aphyolebias peruensis (MYERS, 1954), Austrofundulus (1985). Terminology for osteological structures followed guajira HRBEK, TAPHORN & THOMERSON, 2005, Austro- COSTA (2006); for frontal squamation, HOEDEMAN (1958); fundulus limnaeus SCHULTZ, 1949, Austrofundulus tran- for cephalic neuromast series, COSTA (2001); for brain silis MYERS, 1932, Gnatholebias hoignei (THOMERSON, morphology, EASTMAN & LANOO (2003); and for striated 1974), Gnatholebias zonatus (MYERS, 1935), Llanolebias muscles, WINTERBOTTOM (1974). Distribution of character stellifer (THOMERSON & TURNER, 1973), Micromoema xi- states of morphological characters among terminal ta[a pho phora (THOMERSON & TAPHORN, 1992), Moema pi- appears in Appendi[ 2. The phylogenetic analysis was riana COSTA, 1989, Moema staecki (SEEGERS, 1987), carried out with ma[imum parsimony (MP), performed Neo fundulus ornatipinnis MYERS, 1935, Neofundulus with TNT 1.1 (GOLOBOFF et al., 2008), using the ‘tradi- pa raguayesis (EIGENMANN & KENNEDY, 1903), Rachovia tional¶ search and setting random ta[on-addition rep- brevis (REGAN, 1912), Pterolebias longipinnis GARMAN, licates to 10, tree bisection-reconnection branch swap- 1895, Pterolebias phasianus COSTA, 1988, Rachovia ping, multitrees in effect, collapsing branches of zero- ma culipinnis (RADDA, 1964), Rachovia pyropunctata length, characters equally weighted, and a ma[imum of TAPHORN & THOMERSON, 1978, Renova oscari THOMERSON 1,000 trees saved in each replicate; branch support was & TAPHORN, 1995, Terranatos dolichopterus (WEITZMAN assessed by bootstrap analysis, using a heuristic search & WOURMS, 1967), Trigonectes aplocheiloides HUBER, with 1,000 replicates. Character states of all morphologi- 1995, Trigonectes balzanii (PERUGIA, 1891), and Tri go- cal characters were treated as unordered and genes were nectes rubromarginatus COSTA, 1990, and 16 out-group analysed giving equal weight to all sites. Molecular and ta[a, Anablepsoides stagnatus (EIGENMANN, 1909), At- morphological data were analysed together and separate- lan tirivulus luelingi (SEEGERS, 1984), Atlantirivulus san- ly using MP; molecular data alone were also analysed ten sis (KÖHLER, 1906), Cynodonichthys tenuis (MEEK, with Ma[imum /ikelihood (M/) methods using M(GA 1904), Cynodonichthys weberi (HUBER, 1992), Fun du lo- 5 (TAMURA et al., 2011). Independent analyses compris- panchax gardneri (BOULENGER, 1911), Krypto lebias mar- ing gene partitions, each encompassing individual genes moratus (POEY, 1880), Laimosemion strigatus (REGAN, or group of contiguous gene sequences were performed 1912), Maratecoara formosa COSTA & BRASIL, 1995, to assess the phylogenetic content of each genetic mark- Maratecoara lacortei (LAZARA, 1991), Melanorivulus er. Habitat preferences were inferred from ¿eld observa- punc tatus (BOULENGER, 1895), Nematolebias whitei (MY- tion made during 16 collecting trips between 1986 and ERS, 1942), Pituna poranga COSTA, 1989, Pa pi lio lebias 2013 in all the main areas within the geographical range bitteri (COSTA, 1989), Plesiolebias aruana (LAZARA, of rachovines. 178 VERTEBRATE ZOOLOGY — 64 (2) 2014 Fig. 1. Ma[imum Parsimony (MP) tree of relationships among 22 species of rachovine killi¿ shes (outgroups not depicted) combining mitochondrial DNA (mt-DNA) sequences (3,339 bp) and 161 morphological characters (tree length 12,728). Numbers near branch are bootstrap values above 50 ; above values for the combined analysis, below values for the Ma[imum /ikelihood analysis of mt-DNA alone, followed
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