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Dna Sequence Data JOURNALOF CRUSTACEANBIOLOGY, 20, SPECIALNUMBER 2: 20-36, 2000 MOLECULAR SYSTEMATICS OF THE GONODACTYLIDAE (STOMATOPODA) USING MITOCHONDRIAL CYTOCHROME OXIDASE C (SUBUNIT 1) DNA SEQUENCE DATA Paul H. Barber and Mark V Erdmann (PHB) Departmentof IntegrativeBiology, University of California,Berkeley, California94720, U.S.A. Presentaddress: Department of Organismaland EvolutionaryBiology, HarvardUniversity, Cambridge, Massachusetts02138, U.S.A. (correspondingauthor (PHB) e-mail: [email protected]); (MVE) Departmentof IntegrativeBiology, University of California,Berkeley, California94720, U.S.A. ABSTRACT A molecular phylogenetic analysis of the stomatopod family Gonodactylidae and selected repre- sentatives of the superfamily Gonodactyloidea was conducted using 649 base pairs of DNA sequence data from mitochondrial cytochrome oxidase C subunit 1 (CO-I). Results showed the family Gon- odactylidae is not monophyletic (P < 0.0001). Within the Gonodactylidae, results are inconclusive as to whether Gonodactylellus, Gonodactylinus, and Gonodactylus represent distinct monophyletic taxa or should be collapsed into a single genus Gonodactylus. Results strongly indicate that Gon- odactylellus is polyphyletic; four of the five Gonodactylellus species examined formed a mono- phyletic clade which was closely related to Gonodactylus and Gonodactylinus, while Gonodactylellus hendersoni was found to be deeply divergent from its congeners and formed a strong monophyletic group with members of Gonodactylopsis and Hoplosquilla. The genus Gonodactylaceus was found to be monophyletic and highly divergent from the other gonodactylid genera. The species Gon- odactylaceus aloha is shown to be a synonym of G. mutatus. Finally, although our analysis sug- gests a close relationship of Odontodactylus and Hemisquilla, high levels of nucleotide substitu- tion saturationprevented the resolution of deep (family level) branches within the phylogenetic struc- ture of this relatively old stomatopod lineage. Stomatopods are benthic marine crus- stomatopodfamilies and superfamilieswhich taceans of the class Malacostraca,subclass are now recognized. We present this paper Hoplocarida.Commonly known as mantis in his honor. shrimps,they are both behaviorallycomplex Withinthe five superfamiliesof extantsto- andtaxonomically diverse. More than 400 ex- matopods,the Gonodactyloideahave received tant species are currentlyrecognized from much attentionrecently owing to their com- over 100 genera, representing 19 families plex ecology, elaboratebehavioral repertoire arrangedinto 5 superfamilies:Bathysquil- (Caldwell, 1988, 1991), acute color vision loidea Manning,Squilloidea Latreille, Eryth- (Cronin and Marshall, 1989), and potential rosquilloidea Manning and Bruce, Ly- for use as bioindicatorsof marinepollution siosquilloidea Geisbrecht,and Gonodactyl- stress (Erdmannand Caldwell, 1997). The oidea Geisbrecht(Manning, 1995; Ahyong, Gonodactyloideaare highly diverse; Manning 1997). Alpha taxonomy of the stomatopods (1995) recognized 33 genera in nine gon- has intensified greatly in the past half-cen- odactyloidfamilies. This grouphas the high- tury; by comparison, Kemp (1913) recog- est familialdiversity within the five extantsu- nized only 126 species in 6 genera,all in the perfamiliesand is second only to the Squil- family Squillidae Latreille. While this in- loidea in both species and generic diversity crease in our understandingand appreciation (Manning, 1995). Additionally, the Gon- of stomatopoddiversity and systematicshas odactyloideais a relativelyold lineage. Like been partlya resultof increasedsampling in- the othersuperfamilies, the Gonodactyloidea tensity in cryptichabitats, it is perhapsmost is considered to have Cretaceous origins attributableto the tireless work of Raymond (Schram,1986; Hof, 1998).The oldestknown Manning,who has singly, or with coauthors, fossil stomatopodassigned to one of the ex- described approximately one half of all tant superfamilies,Palaeosquilla brevicoxa known stomatopodspecies and is largely re- Schram, is believed to be a gonodactyloid sponsible for the systematic frameworkof from the middle Cretaceous(Schram, 1968). 20 BARBERAND ERDMANN:MOLECULAR SYSTEMATICS OF THE GONODACTYLIDAE 21 Of the nine recognized gonodactyloid fam- 1981) as a distinct species from G. mutatus ilies, the type family Gonodactylidae is by far (Lanchester, 1903). the most diverse, with ten described genera. Taxonomic revisions have been common in MATERIALSAND METHODS the Gonodactylidae. Manning (1995) split the Taxon Sampling formerly speciose genus of Gonodactylus into Samples were obtained from 33 individuals of 28 five genera: Gonodactylaceus, Gonodactylel- species within the superfamily Gonodactyloidea (Table lus, Gonodactylinus, Gonodactylus, and Neo- 1). Within the family Gonodactylidae, 17 species repre- although he expressed reser- senting seven of the ten described genera in the family gonodactylus, were sampled (Gonodactylaceus Manning n = 3; Gono- vation with regard to the phylogenetic basis dactylellus Manning n = 5; Gonodactylinus Manning n for this division. Recently, Erdmann and = 1; Gonodactylopsis Manning n = 1; Gonodactylus Manning (1998) described five new species Berthold n = 4; Hoplosquilla Holthuis n = 1; Neogono- = of gonodactylid from Indonesia. dactylus Manning n 2). Additionally, taxa from five of within the eight other recognized families within the Gon- Although evolutionary relationships odactyloidea were included (Table 1). A representative the Stomatopoda have been implicitly pro- of the Lysiosquilloidea (Parvisquilla multituberculata posed in systematic descriptions and even Borradaille), recognized by Ahyong (1997) as a sister explicitly discussed in a number of studies clade to the Gonodactyloidea, was included as an out- (e.g., Brooks, 1886; Schram, 1986; Manning, group taxon. Finally, multiple samples of several species (Gonodactylaceus mutatus Lanchester n = 2, Gono- 1969a), modern cladistic methods (using dactylellus hendersoni Manning n = 2, and Gonodacty- morphological data) have only recently been lus childi Manning n = 4) were included to examine the applied to the analysis of stomatopod phy- depth of divergence between geographically distant pop- logenetics (Ahyong, 1997; Hof, 1998). Al- ulations of the same species. Note that although Man- several workers are in- ning (1995) synonymized G. childi as being based on though currently Gonodactylellus incipiens (Lanchester), it has since been volved in extending cladistic techniques to clearly shown to represent a distinct species (Erdmann, stomatopods using molecular sequencing 1997; Erdmann and Manning, in prep.). data (Ahyong, in prep.; Harling, in prep.), the DNA Extraction,Amplification, and Sequencing present paper is the first to attempt a molec- ular phylogenetic analysis of the Gono- Total DNA was extracted from abdominal wall mus- cle tissue of specimens preserved in 70-95% ethanol, us- dactylidae. ing a 5% Chelex? (Biorad) solution (Walsh et al., 1991). In the last ten years the use of mitochon- For those specimens where fresh tissue was available (in- drial DNA sequence data in systematics has dicated in Table 1), a single pereiopod was clipped from become commonplace. Molecular data have living specimens, and mitochondrial DNA was extracted been used to corroborate and purified using Wizard Minipreps? (Promega Corpo- morphological sys- ration) following the methods of Beckman et al. (1993). tematics and taxonomy as well as help resolve A 649 bp fragment of the mitochondrial cytochrome questions unanswered by morphological stud- oxidase-1 gene was amplified via the polymerase chain ies (e.g., Brown et al., 1994; Arndt et al., reaction (Saiki et al., 1988) using primers HCO-2193 and 1996; Itagaki et al., 1998). DNA sequence LCO-1490 designed by Folmer et al. (1994). Hot-start thermocycling was done in a Perkin-Elmer 9600 using data from CO-I has been used in systematic Amplitaq Gold? (Perkin-ElmerCorp.) and began with an studies ranging from family- to subspecies- initial 10-min denaturation at 94?C to activate the en- level relationships (e.g., Gleason et al., 1997; zyme, followed by 42 cycles of 94?C/1 min, 45?C/1 min, Davis et al., 1998; Foighil et al., 1998) and 72?C/1.5 min, and finished with a 3-min final extension at 72?C. Double-stranded PCR were elec- even (e.g., Juan products intraspecific phylogeography trophoresed on TAE agarose gels then excised from the et al., 1998). This study applies molecular gel and purified with Ultraclean 2? (Invitrogen). Cleaned systematic techniques to questions of sto- PCR products were sequenced via cycle sequencing (Am- matopod evolution. The goals of this study plicycle?, Perkin-Elmer Corp.) under manufacturer-rec- P33 are threefold: (1) determine whether phylo- ommended reaction conditions, using radiolabeled d-ATP, followed by electrophoresis and autoradiography. genetic analysis using DNA sequence data supports the currently proposed systematic Data Analyses classification of the Gonodactyloidea in gen- Sequences were manuallyentered into the alignmentpro- eral and the Gonodactylidae in particular; (2) gram Seqapp 1.9 (Gilbert, 1995). Pairwise comparison of evaluate the validity and taxonomic place- sequence variationwas performedusing test version 4.0d64 ment of five new de- of PAUP*, writtenby David Swofford.The presenceof phy- gonodactylid species logenetic signal in the data set was evaluated by examin- scribed in Erdmann and Manning (1998); and ing the skewness of a tree-length distribution of 106 ran-
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