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Freshwater Shrimp–Sponge Association from an Ancient Lake

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Freshwater Shrimp–Sponge Association from an Ancient Lake Biol. Lett. (2007) 3, 262–264 an exceptional shrimp–sponge association in one of doi:10.1098/rsbl.2006.0613 the lakes as the only such record in freshwater further Published online 8 March 2007 confirms the peculiar nature of the lakes’ fauna. Evolutionary biology 2. MATERIAL AND METHODS The shrimp material and the Sulawesi sponges used for this study Freshwater shrimp–sponge were collected in the Malili lakes in September 2003 (by K.v.R. & T.v.R., shrimps and sponges), March 2004 (by T.v.R. & M.G., association from an sponges only), August 2004 (by K.v.R. & T.v.R., shrimps and sponges) and January 2005 (by K.v.R., T.v.R & Y.C., shrimps ancient lake only). Prior to the preservation in 95% ethanol, the shrimp specimens were separated based on substrate and colour pattern, Kristina von Rintelen1,*, Thomas von Rintelen1, which has been photographically documented in the field. Voucher 2 1 3 specimens of shrimps and sponges are deposited in the Museum of Martin Meixner , Carsten Lu¨ ter , Yixiong Cai Natural History, Berlin (ZMB), see electronic supplementary and Matthias Glaubrecht1 material for accession numbers. 1 DNA was extracted exclusively from abdominal tissues Museum of Natural History, Humboldt University, Invalidenstrasse 43, (shrimps) and excised interior tissues (sponges), respectively. For 10115 Berlin, Germany 2 the molecular phylogeny of Caridina, two mitochondrial gene SMB, Services in Molecular Biology, Breitscheidstrasse 70, fragments, 861 bp of the cytochrome oxidase subunit I (COI) and 15562 Ru¨dersdorf, Germany 3 approximately 560 bp of the large ribosomal subunit (16S), were Biodiversity Centre, National Parks Board, 1 Cluny Road, amplified and sequenced on an ABI 3130 DNA sequencer using Singapore 259569, Republic of Singapore Caridina-specific primers COI-F-Car (50-GCTGCTAATTTTAT *Author for correspondence ([email protected]). ATCTACAG-30)andCOI-R-Car(50-TGTGTAGGCATC 0 0 Shrimp–sponge associations occur frequently in TGGGTAATC-3 ), and atyid-specific primers 16S-F-Car (5 -TG CCTGTTTATCAAAAACATGTC-30), 16S-R-Car (50-AGATAG marine ecosystems, serving as model systems AAACCAACCT-GGCTC-30) and 16S-R-Car1 (50-GAAAGATAG for the evolution of eusociality. Here, we AAACTAACCTGGCT-30). For the sponges, the entire nuclear describe the first known instance of such associ- 18S rRNA gene was amplified using primers 18a_mdl (50-AACC ation in freshwater from an ancient lake in TGGTTGATCCTGCCAGT-30) and 18b_mdl (50-TGATCCTT 0 Indonesia. The shrimp Caridina spongicola CTGCAGGTTCACC-TAC-3 ; Medlin et al. 1988). forms an exclusive and probably commensal The orthologous DNA sequences for each group were aligned using default settings, by CLUSTAL W, v. 1.81 (Thompson et al. association with a yet undescribed spongillinid 1994), and optimized by eye. For Caridina, the aligned sequence sponge. Phylogenetic and ecological data suggest sets of COI (781 bp) and 16S (546 bp) were combined into a single a comparatively recent origin of both taxa. alignment after separate analyses yielded congruent topologies. Climatic fluctuations may have facilitated spe- Caridina lanceolata Woltereck, 1937 from the Malili lakes was used ciation and occasional hybridization of the as an outgroup. The alignment of the sponge sequences has a length shrimp species, which is derived from a rock- of 1702 bp and three marine taxa (Spongia officinalis, Mycale fibrexilis and Halichondria melanodocia) were chosen as the outgroup. dwelling ancestor. Their extremely localized The phylogenies have been estimated by Bayesian inference occurrence in an increasingly disturbed area with MRBAYES v. 3.1.2 (Ronquist & Huelsenbeck 2003). Appro- makes both taxa a conservation priority. priate models of sequence evolution were selected using MRMO- DELTEST v. 2.2 (Nylander 2004), and consequently the HKY CIC Keywords: shrimp–sponge association; ancient lake; G model (Caridina) and the GTR CICG (sponges) were employed. recent speciation; ecology; Sulawesi The posterior probabilities of phylogenetic trees were estimated by 1 000 000 (Caridina) and 2 000 000 (sponges) generation Metropo- lis-coupled Markov chain Monte-Carlo algorithms (four chains, chain temperatureZ0.2), with parameters estimated from the 1. INTRODUCTION dataset. A 50% majority-rule consensus tree was constructed following a 50% burn-in (5000 and 10 000 trees, respectively). The Shrimps inhabiting sponges are well known in marine likelihood value plots output by MRBAYES were used to check for ecosystems, and members of different families (e.g. the stationarity of parameters. Alpheidae, Palaeomonidae) form specific, obligate All sequences have been deposited in GenBank; see electronic associations with various sponge species (Arndt supplementary material for accession numbers. 1933). Sponge-dwelling snapping shrimps (Synal- pheus) represent one of the most speciose crustacean 3. RESULTS genera, and have independently evolved eusociality in The recently described decapod freshwater shrimp some species (Macdonald et al. 2006). In contrast to Caridina spongicola (Zitzler & Cai 2006) from one of this well-established marine diversity, no sponge- the Malili lakes of Sulawesi (figures 1b and 2a)isan inhabiting shrimp had so far been found in freshwater. obligate sponge-associate. It dwells exclusively on Here, we describe the first instance of a shrimp– and in a yet undescribed sponge of the suborder sponge association in an ancient lake in Indonesia. Spongillina (figure 2c). The sponge is soft tissued and Ancient lake faunas are outstanding among all can reach a diameter of up to approximately 0.2 m. other freshwater biota owing to their often peculiar Caridina spongicola can occur in high densities, the species, which are usually distinct from that of maximum number of specimens found in a single- surrounding freshwater habitats. The Indonesian dissected sponge was 137 (mean 28.73, nZ15 island Sulawesi has two ancient lake systems sponges examined). Both shrimp and sponge show an (figure 1a), Lake Poso and the Malili lake system, with extreme degree of endemism, being restricted to part typical lacustrine species assemblages and a fair share of the outlet bay (figure 1b) of the largest and the of endemic and unique forms. Among these are a southernmost Malili lake, Lake Towuti, where they cementing bivalve (Rintelen & Glaubrecht 2006) and occur in a depth of 3–5 (K10) m. limpet-like pulmonates that live epibiontic on other The shrimp clade based on data from an mtDNA snails (Albrecht & Glaubrecht 2006). Our discovery of phylogeny (figure 2b) comprises four morphologically Electronic supplementary material is available at http://dx.doi.org/ distinguishable species (C. spongicola, Caridina spinata, 10.1098/rsbl.2006.0613 or via http://www.journals.royalsoc.ac.uk. C. sp. 1 and C. sp. 2), each with a highly specific body Received 6 December 2006 262 This journal is q 2007 The Royal Society Accepted 5 February 2007 Freshwater shrimp–sponge association K. von Rintelen et al. 263 (a)(b) Sulawesi Lake Towuti Lake Poso Towuti Malili outlet bay lake system 5km 100 km Figure 1. The Indonesian island of Sulawesi. (a) The two ancient lake systems of Sulawesi. (b) Occurrence of Caridina spongicola on its sponge host in the outlet bay of Lake Towuti, the largest and the southernmost of the Malili lakes. (b) Caridina lanceolata 97 Caridina spinata Caridina spinata Caridina spinata Caridina spinata 99 100 Caridina sp.1 Caridina spinata Caridina spinata Caridina sp.1 (a) Caridina sp.1 100 Caridina spongicola 100 Caridina spongicola 64 Caridina spongicola Caridina spongicola Caridina sp.2 Caridina sp.2 98 Caridina spongicola Caridina spongicola Caridina sp.1 Caridina spinata Caridina spinata Caridina sp.2 Caridina sp.2 100 Caridina sp.2 96 Caridina sp.1 100 Caridina sp.1 –0.005 Caridina sp.1 (d) 100 Spongillina sp. (c) 100 Spongillina sp. Sulawesi 62 Eunapius fragilis 71 Spongilla lacustris 70 Eunapius carteri Spongillina sp. Sulawesi 86 Lubomirskia abietina Baikalospongia intermedia Swartschewskia papyracea 64 Ephydatia muelleri 93 Ephydatia fluviatilis Ephydatia cooperensis 100 Corvomeyenia sp. Nudospongilla sp. Sulawesi 76 Pachydictium globosum Sulawesi Trochospongilla horrida Trochospongilla pennsylvanica Halichondria melanodocia 100 Mycale fibrexilis Spongia officinalis –0.01 Figure 2. Caridina spongicola and its sponge associate. (a) Caridina spongicola in its natural habitat. Carapace length of adult specimen approximately 1.8–2.8 mm. (b) mtDNA phylogeny of Lake Towuti rock-dwellers (grey box) and sponge-dweller (red) based on 16S and COI (outgroup C. lanceolata). (c) Habitus of Spongillina sp. in the outlet bay of Lake Towuti. (d ) Position of spongillinid species inhabited by shrimps (red arrow) and other Sulawesi sponges (blue) in a nuclear phylogeny of freshwater sponges (grey box) based on 18S. The sponges referred to as Spongillina sp. cannot yet be assigned to a genus within that group. Scale in (b,d ) is substitutions per site. Biol. Lett. (2007) 264 K. von Rintelen et al. Freshwater shrimp–sponge association coloration, but extensively shared haplotypes. All are this side (Chris Lukhaup 2006, personal communi- endemic to Lake Towuti and dwell exclusively, except cation). Protective measures should be taken to ensure for C. spongicola, on hard substrate (rocks). not only the existence of the two beautiful species but With its prominent oscula (figure 2c), the Towuti also to enable further research on the evolution of sponge resembles its marine cousins, but 18S rRNA specialization and interspecific association
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