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Biflagellate Spermatozoon of the Poison-Dart Frogs Epipedobates

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Biflagellate Spermatozoon of the Poison-Dart Frogs Epipedobates JOURNALOFMORPHOLOGY255:114–121(2003) BiflagellateSpermatozoonofthePoison-DartFrogs EpipedobatesfemoralisandColostethussp.(Anura, Dendrobatidae) OdairAguiar–Jr.,1 AdrianA.Garda,1,4 AlbertinaP.Lima,2 GuarinoR.Colli,3 SoˆniaN.Ba´o,4 and ShirleiM.Recco-Pimentel1* 1DepartamentodeBiologiaCelular,InstitutodeBiologia,UniversidadeEstadualdeCampinas,(UNICAMP), 13084-971,Campinas,SP,Brasil 2CoordenadoriadePesquisasemEcologia,InstitutoNacionaldePesquisasdaAmazoˆnia,(INPA),69011-970, Manaus,AM,Brasil 3DepartamentodeZoologiaand 4DepartamentodeBiologiaCelular,InstitutodeCieˆnciasBiolo´gicas,Universidade deBrası´lia,(UnB),70919-970,Brası´lia,DF,Brasil ABSTRACTThisstudydescribesthespermatozoaofthe Manophryne,Phobobates,andAllobates(Myers, dendrobatidsEpipedobatesfemoralisandColostethussp. 1987;ZimmermanandZimmermann,1988;La usinglightandtransmissionelectronmicroscopy.Both Marca,1992,1994). speciespossessabiflagellatespermatozoon,anunusual Colostethusisthelargestdendrobatidgenus,with characteristiconlypreviouslyreportedintwoanuranspe- approximately100describedspecies(Frost,2000). ciesbelongingtothefamiliesLeptodactylidaeand AccordingtoGrantetal.(1997),mostspeciesgroups Racophoridae.Theacrosomalcomplexofbothspeciescon- sistsofaconicalacrosomalvesicleandasubacrosomal ofColostethusarenotfirmlyestablishedbecause cone,bothofwhichcovertheanteriorportionofthenu- theyaredefinedbyacombinationofcharacterstates cleus,buttodifferingextents.Inthemidpiece,thecen- widespreadinothergroups,ratherthanbyunam- triolesaredisposedparalleltoeachotherandtothecell biguoussynapomorphies.SincethegenusCo- axisandgiverisetotwoaxonemes.Twoparaxonemalrods lostethusisdefinedbysymplesiomorphiccharacters, werealsoseenenteringthenuclearfossa.Bothflagella someregarditasparaphyletic(Lynch,1982). aresurroundedbyasinglemitochondrialcollar.Each Epipedobatesisdefinedmainlybyplesiomorphic flagellumisformedbyanaxialfiberconnectedtothe charactersandmayormaynotbeanaturalgroup, axonemebyanaxialsheath;juxta-axonemalfibersare asarguedbyMyers(1987),whopartitionedthe absent.OurdataseemtosupportthatEpipedobatesfemo- genusDendrobates(sensuSilverstone,1975)into ralisshouldbeplacedinaseparatecladepossiblyrelated fournewgenera,includingEpipedobates.Most toColosthetusandthatthesetwogeneramaynotbe speciesofEpipedobateswereformerlyclassified monophyletic.J.Morphol.255:114–121,2003. intoothergenerasuchasDendrobates,Phyllo- ©2002Wiley-Liss,Inc. batesandColostethus(Frost,2000),thusreflect- KEYWORDS:spermultrastructure;biflagellarity;Anura; ingthedifficultyinthetaxonomicassignmentof Dendrobatidae;Epipedobates;Colostethus thesedendrobatids. Variousdatasetshavebeenusedtoinvestigate dendrobatidsystematicrelationships,includingcy- togeneticandmolecularmarkers(Morescalchi, Thesystematicrelationshipsofpoison-dartfrogs 1973;Rasottoetal.,1987;Bogart,1991;Hillisetal., (FamilyDendrobatidae)havebeenstudiedinten- 1993;Hayetal.,1995;Summersetal.,1999;Clough sively(reviewedinFord,1993;Burton,1998).De- andSummers,2000;Vencesetal.,2000)andalso spitethewell-acceptedmonophylyofdendrobatids, theirintergenericaffinitiesremainobscure(Myers etal.,1991;FordandCannatella,1993;Venceset al.,2000).AccordingtoCloughandSummers(2000), Contractgrantsponsor:FAPESP;Contractgrantnumber:Proc. 99/05602-0;Contractgrantsponsor:CNPq;Contractgrantnumber: somemembersofthisfamilycannotbeclassifiedin Proc.300965/00;Contractgrantsponsor:CAPES. anyparticulargenusbecauseoftheabsenceofdiag- nosticcharacters.Theseproblematicspecieshave *Correspondenceto:Dr.ShirleiM.Recco-Pimentel,Departamento undergoneseveraltaxonomicrevisionsthathave deBiologiaCelular,IB,Unicamp,Campinas,SP,Brasil,13084-971. resultedindifferentgenericarrangementsandthe E-mail:[email protected]. creationofnewgenera.Thiswasthecaseofsome Publishedonline00Month2002in speciesformerlyplacedinColostethusandEpipe- WileyInterScience(www.interscience.wiley.com) dobates, but now allocated in Nephelobates, DOI:10.1002/jmor.10052 ©2002WILEY-LISS,INC. BIFLAGELLARITY IN TWO DENDROBATED FROGS 115 Fig. 1. A: The spermatozoa of Epipedobates femoralis showing the presence of two independent flagella, both with an undulating membrane. LM. B: A spermato- cyst of Colostethus sp. where sev- eral pairs of flagella surrounded by mitochondrial collars can be seen. TEM. a, acrosome; f, flagel- lum; LM, light microscopy; mc, mitochondrial collar; n, nucleus; TEM, transmission electron mi- croscopy. Scale bars: A: 10 ␮m; B: 3 ␮m; behavioral characteristics (Zimmermann and Zim- MATERIALS AND METHODS mermann, 1988; Toft, 1995). Such analyses have Two adult male Epipedobates femoralis were collected by Al- been useful in introducing new parameters to com- bertina P. Lima in a 10,000-ha plot of tropical rainforest in the plement the classic morphological traits (Noble, Reserva Florestal Adolfo Ducke, 25 km northeast of Manaus, 1931; Lynch, 1971, 1973; Duellman and Trueb, Amazonas, Brazil (03°08Ј S, 60°04Ј W). Two specimens of Co- 1986; Ford, 1993; Ford and Cannatella, 1993; Bur- lostethus sp. were collected by Janalee P. Caldwell, Laurie J. Vitt, and Robson A. Souza in Guajara´-Mirim, Rondoˆnia, Brazil (10° 19Ј ton, 1998), which can be misleading because of their S, 64° 33Ј W). The specimens of E. femoralis were deposited in the limited number and the ambiguous and erroneous Museu de Histo´ria Natural “Prof. Ada˜o Jose´ Cardoso,” Univer- reporting of some character states (Ford, 1993). sidade Estadual de Campinas, Brazil (ZUEC 11750, 11753), More recently, sperm ultrastructure has been whereas the specimens of Colostethus sp. were deposited in the Sam Noble Oklahoma Museum of Natural History, University of used in phylogenetic analyses of various taxa, in- Oklahoma, USA (OMNH 37001, 37002). cluding fishes (Mattei, 1991; Jamieson and Leung, For light microscopic observations, spermatozoa from 1991), reptiles (Jamieson, 1995; Teixeira et al., glutaraldehyde–paraformaldehyde-fixed smears were stained 1999a,b), platyhelminths (Justine, 1991), and in- with Giemsa (10% pH 6.8) and examined with an Olympus BX60 microscope. For transmission electron microscopy, fragments of sects (Jamieson et al., 1999). Several studies have testes from Epipedobates femoralis and Colostethus sp. were pre- also shown that sperm ultrastructure is also useful fixed in a solution of 2% paraformaldehyde, 2% glutaraldehyde, for phylogenetic inference in anurans (Lee and 3% sucrose, and 5 mM CaCl2 in 0.1 M sodium cacodylate buffer, Jamieson, 1992, 1993; Jamieson et al., 1993; Kwon pH 7.2, at 4°C overnight. The samples were then postfixed for 60 and Lee, 1995; Meyer et al., 1997; Scheltinga et al., min in 1% osmium tetroxide, 0.8% potassium ferricyanide, and 5 mM CaCl2 in 0.1 M sodium cacodylate buffer before staining en 2001). bloc with 0.5% uranyl acetate for 2 h. After dehydration in an In this article we describe the ultrastructure of ascending series of acetone, the samples of E. femoralis were testicular spermatozoa from Epipedobates femoralis embedded in Epon and polymerized at 60°C for 48 h. Alterna- (ϭAllobates femoralis, sensu Zimmermann and Zim- tively, the material of Colostethus sp. was embedded in Spurr resin after the same process of fixation. Ultrathin sections were mermann, 1988) and Colostethus sp. We report the stained with uranyl acetate (3% in water) for 30 min and then for presence of two complete flagella in the spermato- 8 min in lead citrate following Reynolds (1963), with three rinses zoon of these species, a feature not previously re- in distilled water after each solution. Grids were examined with ported for other anuran species, although two sim- a LEO 906 or JEOL 100C electron microscopes at 60kV or 80 kV. ple flagella have already been described to one leptodactylid and one racophorid species (Pugin- RESULTS Rios and Garrido, 1981; Wilson et al., 1991; Jamie- son, 1999). Finally, in light of the new data, we also Spermatozoa of Epipedobates femoralis and Co- discuss the affinities of E. femoralis with the genus lostethus sp. contain two flagella that are inserted Colostethus. into a short midpiece (Fig. 1A,B). The nucleus and 116 O. AGUIAR–JR. ET AL. Fig. 2. Spermatozoa of Co- lostethus sp. A: Longitudinal sec- tion of the acrosome showing the end of the acrosomal vesicle (arrowheads). Also note the canal throughout the subacrosomal cone’s length and the nuclear space. B–E: Transverse sections of the headpiece showing reduction of the acrosomal vesicle and sub- acrosomal cone and progressive enlargement of the nucleus. F: In- sertion of both paraxonemal rods independently in the nuclear fossa of a spermatid. G,H: Implantation of both axonemes in the nuclear fossa and the corresponding par- allel centrioles in the nuclear fossa. I: Insertion of the auxiliary fibers in the nuclear fossa showing the coalescence of the fibers form- ing the paraxonemal rod near the insertion. The paraxonemal rod penetrates the nuclear fossa only slightly (arrowhead). J-L: Trans- verse sections of the tail showing the presence of the mitochondrial collar proximally and its subse- quent disappearance, as well as the reduction in the length of the undulating membrane. Note the constant curved shape of the axial fiber. a, acrosomal vesicle; af, ax- ial fiber; as, axial sheath; ax, ax- oneme; c, centriole; mc, mitochon- drial collar; n, nucleus; nf, nuclear fossa; ns, nuclear space; p, parax- onemal rod; s, subacrosomal ca- nal; sc, subacrosomal cone; u, un- dulating membrane. Scale bars: A–E,G,L: 0.2 ␮m; F,H,I–K: 0.5 ␮m. tail of E. femoralis are approximately 19.5 ␮m and portion of the head and extends to the beginning of 27.0 ␮m long, respectively. The paired flagella
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