Stomatopod Interrelationships: Preliminary Results Based on Analysis of Three Molecular Loci
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Arthropod Systematics & Phylogeny 91 67 (1) 91 – 98 © Museum für Tierkunde Dresden, eISSN 1864-8312, 17.6.2009 Stomatopod Interrelationships: Preliminary Results Based on Analysis of three Molecular Loci SHANE T. AHYONG 1 & SIMON N. JARMAN 2 1 Marine Biodiversity and Biodescurity, National Institute of Water and Atmospheric Research, Private Bag 14901, Kilbirnie, Wellington, New Zealand [[email protected]] 2 Australian Antarctic Division, 203 Channel Highway, Kingston, Tasmania 7050, Australia [[email protected]] Received 16.iii.2009, accepted 15.iv.2009. Published online at www.arthropod-systematics.de on 17.vi.2009. > Abstract The mantis shrimps (Stomatopoda) are quintessential marine predators. The combination of powerful raptorial appendages and remarkably developed sensory systems place the stomatopods among the most effi cient invertebrate predators. High level phylogenetic analyses have been so far based on morphology. Crown-group Unipeltata appear to have diverged in two broad directions from the outset – one towards highly effi cient ‘spearing’ with multispinous dactyli on the raptorial claws (dominated by Lysiosquilloidea and Squilloidea), and the other towards ‘smashing’ (Gonodactyloidea). In a preliminary molecular study of stomatopod interrelationships, we assemble molecular data for mitochondrial 12S and 16S regions, combined with new sequences from the 16S and two regions of the nuclear 28S rDNA to compare with morphological hypotheses. Nineteen species representing 9 of 17 extant families and 3 of 7 superfamilies were analysed. The molecular data refl ect the overall patterns derived from morphology, especially in a monophyletic Squilloidea, a monophyletic Lysiosquilloidea and a monophyletic clade of gonodactyloid smashers. Molecular analyses, however, suggest the novel possibility that Hemisquillidae and possibly Pseudosquillidae, rather than being basal or near basal in Gonodactyloidea, may be basal overall to the extant stomatopods. In this context, it is signifi cant that in many respects, hemisquillids resemble the stem-lineage condition more so than any other extant forms. > Key words Hoplocarida, Stomatopoda, molecular phylogeny. 1. Introduction The mantis shrimps (Stomatopoda) are quintessential well beyond that visible to humans (MARSHALL et al. marine predators and are the most accomplished in 2007). The combination of powerful raptorial append- the Crustacea. Their powerful raptorial appendages, ages and remarkably developed sensory systems place adapted to ‘spearing’ or ‘smashing’ are trademark ad- the stomatopods among the most effi cient invertebrate aptations (CALDWELL & DINGLE 1976). The raptorial predators. strike is one of the fastest known animal movements The evolution of such a potent hunting system is and the force of the blow from the most powerful of considerable interest. The fossil record suggests ‘smashers’ may approach that of a small calibre bul- that the hoplocarid ancestors diverged from other eu- let (PATEK & CALDWELL 2005). An equally important malacostracans during the Devonian, but it was not adaptation enabling the stomatopod to track prey and until the Carboniferous that signs of differentiation engage with its environment is acute vision, which is of the subchelate maxillipeds fi rst appeared (SCHRAM possibly the most complex of any invertebrate. Not 2007). These proto-mantis shrimp groups essentially only is each eye capable of binocular vision, but many form a ‘transition series’ with increasing differentia- species can detect polarised light and wavelengths tion of the second maxilliped as a raptorial claw. The 92 AHYONG & JARMAN: Stomatopod molecular phylogeny claw reaches maximum development in the Unipelta- and Atmospheric Research, Wellington, New Zealand ta, which includes all modern stomatopods, the ‘true’ (NIWA), and Queensland Museum, Brisbane (QM). mantis shrimp. Taxonomic authorities of all terminal taxa are given Unipeltata comprises the Jurassic–Cretaceous in Tab. 1. stem-lineage families Sculdidae Dames, 1886, and The position of Hoplocarida in relation to the oth- Pseudosculdidae Dames, 1886 (see HOF 1998; AHYONG er major malacostracan clades, Leptostraca and Cari- et al. 2007), and the seven extant, crown-group super- doida (= Eumalacostraca of some authors; see MARTIN families (MANNING 1980, 1995; AHYONG & HARLING & DAVIS 2001 for summary) has been subject to some 2000; AHYONG 2001, 2005). Of these seven super- debate. Most recent analyses, however, regard hoplo- families, the bulk of the almost 500 known species caridans as closer to Caridoida than to Leptostraca is contained in three major superfamilies: Gonodac- (e.g., RICHTER & SCHOLTZ 2001; JENNER et al. 2009) tyloidea Giesbrecht, 1910, Lysiosquilloidea Giesbre- with Eumalacostraca comprising hoplocaridans and cht, 1910, and Squilloidea Latreille, 1802. The fossil caridoidans. Although signifi cant amounts of sequence record indicates that these three major superfamilies data are available for both leptostracans and putative- diverged by the late Cretaceous, remaining clearly ly near-basal caridoidans (such as euphausiaceans and recognisable since then. anaspidaceans), only in the case of the leptostracans Phylogenetic analyses of the modern stomato- was sequence data available for all loci studied here- pods have been conducted only in the last decade or in. Therefore, the analysis was rooted to Leptostraca so (e.g., AHYONG 1997; HOF 1998; AHYONG & HARLING based on concatenated sequences of Nebalia sp. (28S: 2000; BARBER & ERDMANN 2000; AHYONG 2005), most AY859590), Nebalia hessleri (12S: AF107606) and of which were based on morphology. AHYONG & HAR- Paranebalia longipes (16S: AY744909). LING’S (2000) comprehensive morphological analysis indicated that Unipeltata diverged in two broad direc- tions from the outset – one towards highly effi cient 2.2. DNA extraction and analysis ‘spearing’ with multispinous dactyli on the raptorial claws, and the other towards ‘smashing’. Although DNA was extracted using a modifi ed Chelex rapid- stomatopods have often been included in wider stud- boiling procedure (WALSH et al. 1991). Approximately ies of arthropod interrelationships (e.g., GIRIBET et al. 0.5 mg of tissue was placed in a 1.5 ml microcentri- 2001; CARAPELLI et al. 2007), only BARBER & ERD- fuge tube containing 200 μl of 6% Chelex® 100 resin MANN (1998), using COI sequences to study species in 50 mM Tris pH 8.0, 0.5 mM EDTA. The tube was and genera within the Gonodactylidae, have directly placed in a 100°C heating block for 5 minutes, vor- applied molecular data to estimate stomatopod phy- texed, incubated for a further 5 minutes at 100°C, and logeny. Thus, the high-level phylogeny of the Sto- then centrifuged at 20,000 × G for 10 minutes. The matopoda has not been specifi cally approached using resulting supernatant was then removed to a fresh 1.5 molecular data. As a prelude to more extensive mo- ml centrifuge tube and was ready as a template for lecular analyses of the stomatopods, the present study PCR amplifi cations. assembles available molecular data for mitochondrial Two regions of the 28S rDNA (df and vx) were 12S and 16S regions, combined with new sequences am plifi ed. The df region was PCR amplifi ed using from the 16S and two regions of the 28S rDNA. the primers 28Sdd (5’-gtcttgaaacagggaccaaggagt ct-3’) and 28Sff (5’-ggtgagttgttacacactccttagtcgg at-3’) (HILLIS & DIXON 1991). The vx region was PCR amplifi ed using the primers 28Sv (5’-aaggtagccaaa 2. Materials and methods tgcctcgtcatc-3’) and 28Sx (5’-gtgaattctgcttcacaatga taggaagagcc-3’) (HILLIS & DIXON 1991). An approxi- mately 530 bp region from the 5’ end of the mito- 2.1. Taxon sampling and outgroup selection chondrial 16S rDNA was amplifi ed using the prim- ers 16Sar-L (5’-cgcctgtttatcaaaaacat-3’) and 16Sbr-H Nineteen species spanning nine families and the larg- (5’-ccggtctgaactcagatcacgt-3’) (PALUMBI et al. 1991). est three superfamilies were included as terminals PCR conditions were identical for all primer sets (Tab. 1). Sequences were derived from GenBank or and took place in 50 μl reactions containing 5 μl of newly gathered. Specimens sequenced for this study Chelex-extracted DNA solution as a template, 0.1% were initially preserved in 85–95% ethanol prior to Triton® X-100, 50 mM KCl, 10 mM Tris-HCl pH DNA extraction. Muscle tissue was sampled from 9.0, 2.5 mM MgCl2, 0.25 mM dNTPs, and 2 units Taq the merus of the raptorial claw or from the abdomen. DNA Polymerase (Promega). Cycle conditions were Voucher specimens are deposited in the Australian 94°C, 30 seconds; 50°C, 1 minute; 72°C, 1.5 minutes Museum, Sydney (AM), National Institute of Water for 40 cycles followed by 72°C, 6 minutes. Complet- Arthropod Systematics & Phylogeny 67 (1) 93 Tab. 1. Terminal taxa, classifi cation, voucher catalogue numbers, and GenBank accession numbers. Voucher specimens for new sequences were deposited in the Australian Museum, Sydney (AM), National Institute of Water and Atmospheric Research (NIWA) and Queensland Museum (QM). New sequences are indicated*. Note that Chorisquilla tweediei sequences (AF107609, AF 107598) are incorrectly listed on GenBank as C. trigibbosa, and Hemisquilla californiensis (AF107597, AF107616) as H. ensigera. Taxon Voucher 12S 16S 28Sdf 28Svx Hoplocarida Calman, 1904 Stomatopoda Latreille, 1817 Gonodactyloidea Giesbrecht, 1910 Hemisquillidae Manning, 1980 Hemisquilla australiensis Stephenson, 1967 AM P56794 — FJ871141* FJ871156* FJ871148* Hemisquilla californiensis Stephenson, 1967 AF107597 AF107616 — — Gonodactylidae