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Multiple host switching events shape the evolution of symbiotic palaemonid shrimps (Crustacea: Decapoda)

. 2016 Jun 01 ; 6 () : 26486. [epub] 20160601

Language English Country Great Britain, England Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

The majority of the almost 1,000 species of Palaemonidae, the most speciose family of caridean shrimp, largely live in symbioses with marine invertebrates of different phyla. These associations range from weak epibiosis to obligatory endosymbiosis and from restricted commensalism to semi-parasitism, with the specialisation to particular hosts likely playing a role in the diversification of this shrimp group. Our study elucidates the evolutionary history of symbiotic palaemonids based on a phylogenetic analysis of 87 species belonging to 43 genera from the Indo-West Pacific and the Atlantic using two nuclear and two mitochondrial markers. A complementary three-marker analysis including taxa from GenBank raises this number to 107 species from 48 genera. Seven larger clades were recovered in the molecular phylogeny; the basal-most one includes mostly free-living shrimp, albeit with a few symbiotic species. Ancestral state reconstruction revealed that free-living forms likely colonised cnidarian hosts initially, and switching between different host phyla occurred multiple times in palaemonid evolutionary history. In some cases this was likely facilitated by the availability of analogous microhabitats in unrelated but morphologically similar host groups. Host switching and adaptations to newly colonised host groups must have played an important role in the evolution of this diverse shrimp group.

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Dimijian G. G. Evolving together: the biology of symbiosis, part 1. BUMC Proceedings 13, 217–226 (2000). PubMed PMC

Sapp J. The dynamics of symbiosis: an historical overview. Can. J. Bot. 82, 1046–1056 (2004).

Leung T. L. F. & Poulin R. Parasitism, commensalism, and mutualism: Exploring the many shades of symbioses. Vie milieu 58, 107–115 (2008).

De Grave S. Biogeography of Indo-Pacific Pontoniinae (Crustacea, Decapoda): a PAE analysis. J. Biogeogr. 28, 1239–1253 (2001).

Bruce A. J. Shrimps and prawns of coral reefs, with special reference to commensalism, in Geology of Coral Reefs (eds Jones O. A. & Endean R.) 37–94 (Academic Press, 1976).

De Grave S., Fransen C. H. J. M. & Page T. J. Let’s be pals again: major systematic changes in Palaemonidae (Crustacea: Decapoda). PeerJ 3, e1167 (2015). PubMed PMC

De Grave S. & Fransen C. H. J. M. Carideorum catalogus: the recent species of the dendrobranchiate, stenopodidean, procarididean and caridean shrimps (Crustacea: Decapoda). Zool. Meded. 85, 195–589 (2011).

Fransen C. H. J. M. On Pontoniinae (Crustacea, Decapoda, Palaemonidae) collected from ascidians. Zoosystema 28, 713–746 (2006).

Bruce A. J. & Okuno J. Periclimenes dardanicola n. sp., a new species of hermit crab associated shrimp (Crustacea, Decapoda, Palaemonidae) from the western Pacific. Zoosystema 28, 367–377 (2006).

Fautin D. G., Guo C.-C. & Hwang J.-S. Costs and benefits of the symbiosis between the anemoneshrimp Periclimenes brevicarpalis and its host Entacmaea quadricolor. Mar. Ecol. Prog. Ser. 129, 77–84 (1995).

Ďuriš Z., Horká I., Juračka P. J., Petrusek A. & Sandford , F. These squatters are not innocent: the evidence of parasitism in sponge-inhabiting shrimps. PLoS ONE 6, e21987 (2011). PubMed PMC

Dobson N. C., De Grave S. & Johnson M. L. Linking eye design with host symbiont relationships in pontoniine shrimps (Crustacea, Decapoda, Palaemonidae). PLoS ONE 9, e99505 (2014). PubMed PMC

Millanes A., Truong C., Westberg M., Diederich P. & Wedin M. Host switching promotes diversity in host-specialized mycoparasitic fungi: uncoupled evolution in the Biatoropsis-Usnea system. Evolution 68, 1576–1593 (2014). PubMed

de Vienne D. M. et al. Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytol. 198, 347–385 (2013). PubMed

Hoberg E. P. & Brooks D. R. A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. J. Biogeogr. 35, 1533–1550 (2008).

Gómez J. M., Verdú M. & Perfectti F. Ecological interactions are evolutionarily conserved across the entire tree of life. Nature 465, 918–921 (2010). PubMed

Goto R., Kawakita A., Ishikawa H., Hamamura Y. & Kato M. Molecular phylogeny of the bivalve superfamily Galeommatoidea (Heterodonta, Veneroida) reveals dynamic evolution of symbiotic lifestyle and interphylum host switching. BMC Evol. Biol. 12, 172 (2012). PubMed PMC

Sotka E. Local adaptation in host use among marine invertebrates. Ecol. Lett. 8, 448–459 (2005).

Lanterbecq D., Rouse G. W. & Eeckhaut I. Evidence for cospeciation events in the host–symbiont system involving crinoids (Echinodermata) and their obligate associates, the myzostomids (Myzostomida, Annelida). Mol. Phylogenet. Evol. 54, 357–371 (2010). PubMed

Spencer H. G. Using phylogenies to reveal rare events. New Zealand Sci. Rev. 66, 9–11 (2009).

Kou Q., Li X. Z., Chan T.-Y. & Chu K. H. Divergent evolutionary pathways and host shifts among the commensal pontoniine shrimps: a preliminary analysis based on selected Indo-Pacific species. Org. Divers. Evol. 15, 369–377 (2015).

Gan Z. B., Li X., Chan T.-Y., Chu K. H. & Kou Q. Phylogeny of Indo-West Pacific pontoniine shrimps (Crustacea: Decapoda: Caridea) based on multilocus analysis. J. Zoolog. Syst. Evol. Res. 53, 282–290 (2015).

Okuno J. A new species of cnidarian-associated shrimp of the genus Cuapetes Clark, 1919 (Decapoda, Palaemonidae) from Suruga Bay, Japan, in Studies on Eumalacostraca: a homage to Masatsune Takeda (eds Komatsu H., Okuno J. & Fukuoka K.) Crustac. Monogr. 17, 1–325 (2012).

Okuno J. & Bruce A. J. Designation of Ancylomenes gen. nov., for the ‘Periclimenes aesopius species group’ (Crustacea: Decapoda: Palaemonidae), with the description of a new species and a checklist of congeneric species, in Contributions to shrimp taxonomy (eds De Grave S. & Fransen C. H. J. M.). Zootaxa 2372, 1–414 (2010).

Bruce A. J. The hosts of the coral-associated Indo-West Pacific Pontoniine shrimps. Atoll Res. Bull. 205, 1–19 (1977).

Okuno J. & Chan T.-Y. A new antipatharian-associated species of the genus Cuapetes Clark, 1919 (Crustacea: Decapoda: Palaemonidae) and a new record of C. nilandensis (Borradaile, 1915) from Japan, in Scientific Results of the Marine Biodiversity Expedition - KUMEJIMA 2009 (eds Naruse T., Chan T.-Y., Tan H. H., Ahyong S. T. & Reimer J. D.) Zootaxa 3367, 1–280 (2012).

Marin I. & Britayev T. Symbiotic community, associated with corals of the genus Galaxea Oken, 1815 (Euphyllidae: Scleractinia) 148 (KMK Scientific Press, 2014).

Bruce A. J. The shrimps associated with Indo-West Pacific echinoderms, with the descriptions of a new species in the genus Periclimenes Costa, 1844 (Crustacea: Pontoniinae). Mem. Aust. Mus. 16, 191–216 (1982).

Bruce A. J. Notes on some Indo-Pacific Pontoniinae XLVL. Palaemonella foresti sp. nov., a new pontoniine shrimp from Western Australia (Decapoda, Palaemonidae), with a review of the Indo-West Pacific species of the genus Palaemonella Dana, 1852. Crustaceana 75, 277–298 (2002).

Bruce A. J. Ancylomenes australis sp. nov. (Crustacea: Decapoda: Pontoniinae) from South Africa. Zootaxa 3722, 73–82 (2013). PubMed

Limbaugh C., Pederson H. & Chace F. A. Jr. Shrimps that clean fishes. Bull. Mar. Sci. Gulf Caribb. 11, 237–257 (1961).

Caulier G., Lepoint G., Nedervelde F. V. & Eeckhaut I. The diet of the Harlequin crab Lissocarcinus orbicularis, an obligate symbiont of sea cucumbers (holothuroids) belonging to the genera Thelenota, Bohadschia and Holothuria. Symbiosis 62, 91–99 (2014).

Titgen R. H. Gnathophyllid shrimp of the Hawaiian Islands, with the description of a new species of Gnathophyllum (Decapoda, Gnathophyllidae). Crustaceana 56, 200–210 (1989).

Ahyong S. T. Gnathophyllum taylori, a new species of caridean shrimp from south-eastern Australia (Crustacea: Decapoda: Gnathophyllidae). Mem. Mus. Victoria 60, 237–242 (2003).

Prakash S. & Kumar T. T. A. Feeding behavior of Harlequin shrimp Hymenocera picta Dana, 1852 (Hymenoceridae) on sea star Linckia laevigata (Ophidiasteridae). J. Threat. Taxa 5, 4819–4821 (2013).

Fransen C. H. J. M. & Goud J. Chromodoris magnifica (Quy & Gaimard, 1832), a new nudibranch host for the shrimp Periclimenes imperator Bruce, 1967 (Pontoniinae). Zool. Meded. 73, 273–283 (2000).

Fransen C. H. J. M. & Hoeksema B. W. Going for the stars: extending the host record for the reef-dwelling Emperor shrimp, Periclimenes imperator (Pontoniinae). Mar. Biodivers. 44, 465–466 (2014).

Li X. & Bruce A. J. Further Indo-West Pacific palaemonoid shrimps (Crustacea: Decapoda: Palaemonoidea), principally from the New Caledonian region. J. Nat. Hist. 40, 611–738 (2006).

Bruce A. J. Crustacea Decapoda: Further deep-sea palaemonoid shrimps from New Caledonian waters in Résultats des Campagnes MUSORSTOM (ed. Crosnier A.). Mem. Mus. Nat. Hist. Nat., Nouv. Ser. A 152, 299–411 (1991).

De Grave S. & Anker A. A new species of Periclimenes Costa from Utila, Honduras (Crustacea, Decapoda, Pontoniinae). Ann. Naturhist. Mus. Wien 110B, 139–148 (2009).

Fransen C. H. J. M. Taxonomy, phylogeny, historical biogeography, and historical ecology of the genus Pontonia (Crustacea: Decapoda: Caridea: Palaemonidae). Zool. Verh. 336, 1–433 (2002).

Kou Q. et al. Phylogenetic relationships among genera of the Periclimenes complex (Crustacea: Decapoda: Pontoniinae) based on mitochondrial and nuclear DNA. Mol. Phylogenet. Evol. 68, 14–22 (2013). PubMed

Folmer O., Black M., Hoeh W., Lutz R. & Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994). PubMed

Palumbi S. R. et al. The simple fool’s guide to PCR (University of Hawaii, 1991).

Colgan D. J., Hutchings P. A. & Beacham E. Multi-gene analyses of the phylogenetic relationships among the Mollusca, Annelida, and Arthropoda. Zool. Stud. 47, 338–351 (2008).

Whiting M. F. Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zool. Scr. 31, 93–104 (2002).

Li C. P., De Grave S., Lei H. C., Chan T.-Y. & Chu K. H. Molecular systematics of caridean shrimps based on five nuclear genes: Implications for superfamily classification. Zool. Anz. 250, 270–279 (2011).

Edgar R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004). PubMed PMC

Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013). PubMed PMC

Xia X. Assessing substitution saturation with DAMBE, in The Phylogenetic Handbook: A Practical Approach to Phylogenetic Analysis and Hypothesis Testing (eds Lemey P. et al.) 615–630 (Cambridge University Press, 2009).

Xia X. H., Xie Z., Salemi M., Chen L. & Wang Y. An index of substitution saturation and its application. Mol. Phyl. Evol. 26, 1–7 (2003). PubMed

Talavera G. & Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564–577 (2007). PubMed

Vaidya G., Lohman D. J. & Meier R. SequenceMatrix: concatenation software for the fast assembly of multigene datasets with character set and codon information. Cladistics 27, 171–180 (2011). PubMed

Lanfear R., Calcott B., Ho S. Y. W. & Guindon S. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695–1701 (2012). PubMed

Miller M. A., Pfeiffer W. & Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees, in Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA, 1–8 (2010).

Ronquist F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012). PubMed PMC

Stamatakis A. RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014). PubMed PMC

Letunic I. & Bork P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39, 1–4 (2011). PubMed PMC

Rambaut A. FigTree version 1.4.2. (2009). Available at: http://tree.bio.ed.ac.uk (Accessed: 10th April 2016).

Maddison W. P. & Maddison D. R. Mesquite: a modular system for evolutionary analysis. Version 3.04. (2015). Available at: http://mesquiteproject.org (Accessed: 30th November 2015).

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