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Molecular Phylogeny and Diversification of Freshwater Shrimps

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Molecular Phylogeny and Diversification of Freshwater Shrimps Available online at www.sciencedirect.com Molecular Phylogenetics and Evolution 45 (2007) 1033–1041 www.elsevier.com/locate/ympev Molecular phylogeny and diversification of freshwater shrimps (Decapoda, Atyidae, Caridina) from ancient Lake Poso (Sulawesi, Indonesia)—The importance of being colourful Kristina von Rintelen *, Thomas von Rintelen, Matthias Glaubrecht Museum of Natural History, Humboldt University Berlin, Invalidenstrasse 43, 10115 Berlin, Germany Received 2 April 2007; revised 23 June 2007; accepted 1 July 2007 Available online 12 July 2007 Abstract Ancient Lake Poso on the Indonesian island Sulawesi hosts a highly diverse endemic fauna, including a small species flock of atyid Caridina shrimps, which are characterized by conspicuous colour patterns. We used a mtDNA based molecular phylogeny to test the assumption of a monophyletic origin and intralacustrine radiation of the species flock and to assess the species specificity of some colour morphs. Our data reveal a rapid radiation of Caridina in the entire Poso drainage system, but provide no strong evidence for a mono- phyletic radiation of the lake species. Nevertheless each lacustrine species shows a varying degree of substrate or trophic specialization, usually considered a hallmark of adaptive radiation. Two distinct colour forms previously attributed to a single species, C. ensifera, lack distinguishing qualitative morphological characters, but are shown to be two different species. In contrast, morphologically rather dis- tinct lake species lacking specific colour patterns may be hybridizing with riverine taxa. These results suggest that colour may play a similar role in species recognition and possibly speciation in ancient lake Caridina as hypothesized, e.g. for some African cichlids. Ó 2007 Elsevier Inc. All rights reserved. Keywords: Ancient lakes; Molecular phylogeny; Adaptive radiation; Colour; Cryptic species; Sulawesi 1. Introduction the lake has only been tested for two mollusc species flocks, and been supported for the pachychilids, but rejected for Ancient lakes, with their often highly diverse and speci- corbiculid bivalves (Rintelen and Glaubrecht, 2006). ose endemic fauna, are fertile grounds for the study of The freshwater shrimp genus Caridina H. Milne diversification processes, particularly speciation. Intrala- Edwards, 1837 (Decapoda, Atyidae) is represented in custrine and adaptive radiation is generally regarded as Lake Poso and its catchment by currently three described the major mode of origin of ancient lake species flocks species: C. ensifera Schenkel, 1902 and C. sarasinorum (e.g. Martens, 1997; Rossiter and Kawanabe, 2000; Fryer, Schenkel, 1902 from the lake itself and Caridina acutiros- 2006). The fauna of ancient Lake Poso in the central high- tris Schenkel, 1902 from surrounding rivers (Schenkel, lands of the Indonesian island Sulawesi (Fig. 1) comprises a 1902; Chace, 1997). All three are morphologically dis- fascinating and rich assemblage of endemic freshwater tinct, possessing the typical feeding appendages (cheli- organisms with several species flocks, e.g. ricefishes (Paren- peds) associated with a characteristic feeding behaviour ti and Soeroto, 2004), hydrobioid gastropods (Haase and described for Caridina (Fryer, 1960), i.e. small food par- Bouchet, 2006) and pachychilid gastropods (Rintelen ticles are swept from the substrate by the setae of the et al., 2004). The hypothesis of an adaptive radiation in very mobile chelipeds and are passed with extreme rapid- ity to the mouthparts. Schenkel (1902) already mentioned * differences in the cheliped morphology between C. ensif- Corresponding author. Fax: +49 30 20938565. E-mail address: [email protected] (K. von era and C. sarasinorum, e.g. stouter chelae of the first Rintelen). chelipeds in the latter. 1055-7903/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2007.07.002 1034 K. von Rintelen et al. / Molecular Phylogenetics and Evolution 45 (2007) 1033–1041 Fig. 1. Sulawesi and Lake Poso, sampling and colour morphs (see Table 1 for further details). (a) Sulawesi, sampling sites outside of Lake Poso. (b) Lake Poso and catchment, lacustrine (white dots; L1–17) and riverine sampling sites (black dots; R1–11). (c) and (d) C. ensifera colour morphs, enframed tailfans are shown in detail: ‘‘blue’’ with an elongated blue patch on the distal part of each endopod (upside down V-shape); ‘‘red’’ smaller red spot on the distal part of each exopod. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Besides the differences in trophic morphology, i.e. the system of Sulawesi, or C. trifasciata Yam and Cai, 2003 chelipeds, the most characteristic feature of Lake Poso from Hong Kong (Yam and Cai, 2003), species specificity Caridina is the conspicuous body colouration recently dis- has been doubted in other cases, such as for the striking covered by field observation of living specimens (Rintelen colour forms of some widespread species used in aquarium and Rintelen, pers. observ.). One species in particular, Car- trade (for example the Caridina serrata species group; idina ensifera, not only shows the most obvious colour pat- Andreas Karge and Werner Klotz, pers. comm.). The lack tern among all species in the lake, but is the only one with of a well-established taxonomy in Caridina is a major two easily distinguishable colour morphs (‘‘red’’ and obstacle in this respect, and species distinction is often dif- ‘‘blue’’; Fig. 1c, d), which have not been reported before. ficult. Recent studies using molecular data indicate, how- The respective pattern is equally pronounced in both sexes ever, that morphologically cryptic species among atyid and already distinctive in juveniles. This observation is a shrimps may be common as for instance shown in Austra- priori equally compatible with the assumption of intraspe- lian Caridina (Page et al., 2005). cific polymorphism or the existence of ‘cryptic’ species. Whereas the lack of data in Caridina prevents the study While Caridina is known to show species specific colour of the evolutionary role of body colouration, it is a well- patterns in some taxa, for example C. spongicola from the documented feature in the lacustrine radiations of fishes, Malili lakes (Zitzler and Cai, 2006), the second ancient lake especially African cichlids, with regard to its potential K. von Rintelen et al. / Molecular Phylogenetics and Evolution 45 (2007) 1033–1041 1035 importance in speciation and radiation (e.g. Danley and Inference (BI) with MrBayes 3.1 (Ronquist and Huelsen- Kocher, 2001; Seehausen and Schluter, 2004; Genner and beck, 2003). MP analyses were done with indels coded as Turner, 2005). fifth base and using a full heuristic search with random Here, we use a molecular phylogeny in combination addition (100 repetitions) and tree bisection–reconnection, with morphological and ecological data (i) to test the gen- the same settings were used in a MP bootstrap analysis eral assumption of an adaptive radiation for Lake Poso (1000 replicates). For the ML and BI analyses the appro- Caridina; (ii) to seek molecular support for morphology- priate models of sequence evolution (GTR + I + C for based species descriptions and for yet undescribed forms COI and the HKY + I + C for 16S) were selected using found in new samples, in particular (iii) to investigate the MrModeltest 2.2 (Nylander, 2004) both by Likelihood significance of the two colour morphs of C. ensifera.In Ratio Tests and based on the Aikaike Information Crite- order to achieve the first aim, we use the definition of rion. The two genes were set as partitions in the concate- Schluter (2000) and apply the phylogenetic (common nated dataset and analyses run with the model specified ancestry and rapid speciation) and ecological (phenotype- for each partition separately. The ML analysis was done environment correlation) criteria he proposed to detect with Treefinder default settings, and 1000 bootstrap repli- an adaptive radiation. cates. For the BI analysis posterior probabilities of phylo- genetic trees were estimated by a 2,000,000 generation 2. Materials and methods Metropolis-coupled Markov chain Monte Carlo algorithm (4 chains, chain temperature = 0.2), with parameters esti- Material from Lake Poso (17 localities) and its drainage mated from the dataset. A 50% majority-rule consensus (11 localities) was sampled by the authors in March and tree was constructed following a 50% burn-in (10,000 trees) August 2004 and October 2005 (Fig. 1b and Table 1). to allow likelihood values to reach stationarity, which was Comparative samples were collected in other parts of assessed using the value plots output by MrBayes. Sulawesi (Fig. 1a and Table 1). Prior to preservation in All sequences have been deposited in EMBL Nucleotide 95% ethanol, lacustrine specimens were separated based Sequence Database (EMBL-Bank); see Table 1 for acces- on colour pattern, which has been photographically docu- sion numbers. mented in the field. Voucher specimens are deposited in the Museum of Natural History, Berlin (ZMB); see Table 1 for 3. Results accession numbers. Fourteen morphometric measurements (compare Zitzler 3.1. Species delineation in Lake Poso based on morphology and Cai, 2006) were taken from n = 40 individuals each of both morphs of C. ensifera (see Supplementary Table 2 for Based on the newly collected material we can distinguish details) using a stereo microscope with an ocular microm- five morphologically distinct species (Table 2): three from eter. Scanning electron microscopy was used to study the the lake itself, C. ensifera, C. sarasinorum and C. spec.A, chelipeds from n = 2–5 critical point dried specimens of a new lacustrine species (compare Fig. 1, L1–17), as well each species. as two from the surrounding rivers, C. acutirostris and C. DNA was extracted exclusively from abdominal tissue. spec. B, a yet undescribed riverine species (Fig. 1, R1–11). For the molecular phylogeny two mitochondrial gene frag- As mentioned in the introduction, C. ensifera comprises ments, 861 bp of cytochrome oxidase subunit I (COI) and two colour forms, ‘‘blue’’ and ‘‘red’’ (Fig.
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