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Genetic Population Structures of the Blue Starfish Linckia Laevigata and Its Gastropod Ectoparasite Thyca Crystallina

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Genetic Population Structures of the Blue Starfish Linckia Laevigata and Its Gastropod Ectoparasite Thyca Crystallina Vol. 396: 211–219, 2009 MARINE ECOLOGY PROGRESS SERIES Published December 9 doi: 10.3354/meps08281 Mar Ecol Prog Ser Contribution to the Theme Section ‘Marine biodiversity: current understanding and future research’ OPENPEN ACCESSCCESS Genetic population structures of the blue starfish Linckia laevigata and its gastropod ectoparasite Thyca crystallina M. Kochzius1,*,**, C. Seidel1, 2, J. Hauschild1, 3, S. Kirchhoff1, P. Mester1, I. Meyer-Wachsmuth1, A. Nuryanto1, 4, J. Timm1 1Biotechnology and Molecular Genetics, FB2-UFT, University of Bremen, Leobenerstrasse UFT, 28359 Bremen, Germany 2Present address: Insitute of Biochemistry, University of Leipzig, Brüderstrasse 34, 04103 Leipzig, Germany 3Present address: Friedrich-Loeffler-Institut, Bundesforschungsinstitut für Tiergesundheit, Institut für Nutztiergenetik, Höltystrasse 10, 31535 Neustadt, Germany 4Present address: Faculty of Biology, Jenderal Soedirman University, Dr. Suparno Street, Purwokerto 53122, Indonesia ABSTRACT: Comparative analyses of the genetic population structure of hosts and parasites can be useful to elucidate factors that influence dispersal, because common ecological and evolutionary processes can lead to congruent patterns. We studied the comparative genetic population structure based on partial sequences of the mitochondrial cytochrome oxidase I gene of the blue starfish Linckia laevigata and its gastropod ectoparasite Thyca crystallina in order to elucidate evolutionary processes in the Indo-Malay Archipelago. AMOVA revealed a low fixation index but significant φ genetic population structure ( ST = 0.03) in L. laevigata, whereas T. crystallina showed panmixing φ ( ST = 0.005). According to a hierarchical AMOVA, the populations of L. laevigata could be assigned to the following groups: (1) Eastern Indian Ocean, (2) central Indo-Malay Archipelago and (3) West- ern Pacific. This pattern of a genetic break in L. laevigata between the Indian and Pacific Ocean, con- gruent to studies on other marine species in the Indo-Malay Archipelago, is likely due to allopatry caused by Pliocene and Pleistocene glacial sea level low stands. KEY WORDS: COI · Coral Triangle · Coral reef · Phylogeography · Population expansion · Southeast Asia Resale or republication not permitted without written consent of the publisher INTRODUCTION Warén 1980, Janssen 1985), which penetrates the radial hemal and perihemal system of L. laevigata with Comparative analyses of the genetic population its proboscis to obtain nutrients (Egloff et al. 1988). structure of a host and its parasite can be used to eluci- T. crystallina seems to be co-distributed with its host, date factors that influence dispersal (Criscione 2008), ranging from the Western Indian Ocean across the because common ecological and evolutionary pro- Indo-Malay Archipelago and northeastern Australia to cesses can lead to congruent patterns (Bermingham & Samoa and Fiji (Sloan et al. 1979, Warén 1980). Infec- Moritz 1998, Avise 2000). The blue starfish Linckia tion rates of L. laevigata with T. crystallina vary among laevigata (Ophidiasteridea; Chao 1999) is widely dis- populations, ranging from 14.3% in Fiji (Egloff et al. tributed on Indo-Pacific coral reefs, from the Western 1988), 15.7% (Troncoso & Van Goethem 1998) and Indian Ocean across the Indo-Malay Archipelago to 22.3% (Bouillon & Jangoux 1984) in eastern New southeastern Polynesia (Yamaguchi 1977). It is fre- Guinea to 62.0% in the Moluccas (Elder 1979). quently parasitised by the obligate and strictly specific Here we compare the genetic population structure ectoparasitic gastropod Thyca crystallina (Eulimidae; of the host Linckia laevigata and its parasite Thyca **Email: [email protected] © Inter-Research 2009 · www.int-res.com **All authors except M.K. and C.S. are in alphabetical order 212 Mar Ecol Prog Ser 396: 211–219, 2009 crystallina in the Indo-Malay Archipelago. This highly MATERIALS AND METHODS dynamic region in terms of biodiversity, ecology, geo- logy and oceanography is the centre of marine shal- Sampling. Tissue samples from 270 specimens of the low water biodiversity (Briggs 1999, Hoeksema 2007). blue starfish Linckia laevigata and 324 specimens of its Molecular phylogenetic studies have shown a break ectoparasite, the snail Thyca crystallina, were col- between the Indian and Pacific Oceans, e.g. in lion- lected during several field trips from 2004 to 2007 at fishes (Kochzius et al. 2003), clownfishes (Timm et al. 24 sample sites across the Indo-Malay Archipelago 2008), and damselfishes (Froukh & Kochzius 2008). (Fig. 1A,C, Table 1). Several colour morphs of L. laevi- Additionally, a growing number of population genetic gata are known, such as blue, orange, green, and studies in the Indo-Malay Archipelago show a com- violet. Since genetic studies indicated that colour plex pattern of divergent lineages and restricted gene variation is congruent to genetic variation (Williams & flow, e.g. in a clownfish (Timm & Kochzius 2008), Benzie 1998) and that species boundaries in Linckia giant clams (Kochzius & Nuryanto 2008, Nuryanto & are difficult to define (Williams 2000), only blue colour Kochzius 2009), and a mushroom coral (Knittweis et morphs were analysed. Tissue samples were preserved al. 2009). in >96% ethanol and later stored at 4°C. Plate tectonic movements in the Indo-Malay Archi- DNA extraction, amplification and sequencing. pelago and global fluctuation of sea level during multi- Extraction of genomic DNA from both species was ple Pliocene and Pleistocene glaciations are the pri- done with the Chelex method, following the protocol of mary hypothesised triggers for this genetic separation Walsh et al. (1991). A fragment of the mitochondrial of the 2 ocean basins. Most of the islands in the Indo- COI gene was used for both species as molecular Malay Archipelago did not exist or were not at their marker and amplified with the primers from Folmer et current position about 30 million years ago. During al. (1994). PCR was conducted in a volume of 50 µl and that time, water masses of the Pacific South Equatorial contained 2 µl DNA template, 10 mM Tris-HCl (pH 9), Current (SEC) entered the Indian Ocean via the so- 50 mM KCl, 4 mM MgCl2, 0.4 µM of each primer, called Indonesian seaway. This current pattern started 0.2 mM dNTPs, 2 µl BSA (2 mg/ml) and 1 U Taq poly- to change about 25 million years ago, due to the devel- merase. The following temperature profile was used opment of Sulawesi by the amalgamation of several for the PCR: 94°C for 5 min, followed by 35 cycles of fragments and the northward movement of New 1 min at 94°C, 1.5 min at 45°C and 1 min at 72°C. Final Guinea, the Bird’s Head Peninsula, and Australia (Hall extension was conducted at 72°C for 5 min. The PCR 1998). The Indonesian seaway was finally closed about products were purified using the QIAquick spin col- 5 million years ago by the northward displacement of umn PCR purification kit (Qiagen), following the New Guinea (Cane & Molnar 2001). Since then, the manufacturer’s protocol. Sequencing was done using major exchange of water masses between the 2 oceans the DyeDeoxy terminator chemistry (PE Biosystem) has been facilitated by the Indonesian throughflow and an automated sequencer (ABI PRISM 310 and (ITF), which originates from the northern Pacific (Gor- 3100, Applied Biosystems). New primers were de- don & Fine 1996, Gordon 2005). signed for cycle sequencing in Linckia laevigata Additionally, multiple glaciations in the Pliocene and (Linckia Seq Frw [forward]: 5’-AAA ATC AGA ATA Pleistocene caused global fluctuations in sea level with AGT GCT GGA-3’; Linckia Seq Rev [reverse]: 5’-TTT low stands of up to 120 m below present sea level GGA GCT TGA GCT GGA ATG-3’) and Thyca crystal- (Krantz 1991, Rohling et al. 1998, Siddall et al. 2003). lina (Thyca Seq Frw [forward]: 5’-TAT TGT AAC TGC Shallow shelf areas such as the Sunda shelf were TCA TGC TTT TG-3’). exposed, and ocean basins were separated (Voris 2000; Genetic diversity. Sequences were edited with the Fig. 1). Molecular clock estimates support the view of programmes Sequence Navigator (version 1.0.1, allopatric speciation in separate ocean basins during Applied Biosystems) or Seqman (version 4.05, DNAS- the Pliocene and Pleistocene in some species (Kochzius tar). They were translated to amino acids with the et al. 2003, Timm et al. 2008). program Bioedit (version 7.0.9.0, Hall 1999) in order The present study aims to elucidate if common eco- to exclude mistakes in sequencing and to verify if a logical and evolutionary processes lead to congruence functional mitochondrial DNA sequence was obtained in the genetic structure of Linckia laevigata and Thyca and not a nuclear pseudogene. Multiple alignment crystallina populations from the Indo-Malay Archipel- was done using Clustal W (Thompson et al. 1994) as ago. The genetic marker used for both species in the implemented in the software Bioedit. Haplotype present study is the cytochrome c oxidase I gene (COI), diversity h (Nei 1987) and nucleotide diversity (Nei & which is suitable to investigate the genetic population Jin 1989) were calculated with the programme structure of starfishes (e.g. Harley et al. 2006) and Arlequin (http://cmpg.unibe.ch/software/arlequin3, snails (e.g. Reid et al. 2006). version 3.11; Excoffier et al. 2005). Linckia laevigata Thyca crystallina A C Ce AS Mindanao Mindanao Eddy Eddy BI NECC BI NECC KK ITF NB ITF Sa Ma LS Halmahera Sa Ma LS Halmahera Eddy Eddy SEC SEC Borneo TI Borneo TI N Maluku Mi Bk N Maluku Bk Lu Sea Pi Lu Sea Do Do Mi Sumatra Sulawesi Ke New Sumatra Sulawesi Ke New PS Sp Guinea PS Sp Guinea Kochzius etal.:Geneticstructure ofhostandectoparasite SSP Se SSP Banda Banda Ka Bi Ka Bi Sea Sea Java ITF Java ITF ITF ITF Ko Ku Ko Ku imor 0 Sumba T 0 Ba Sumba Timor ITF ITF B D Fig. 1. Linckia laevigata (A, B) and Thyca crystallina (C, D). (A, C) Indo-Malay Archipelago with sample sites (for abbreviations see Table 1) as well as oceanographic pat- terns with dominant (solid lines) and seasonally changing (dashed lines) currents (Wyrtki 1961, Gordon & Fine 1996, Gordon 2005).
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