Palaemonidae is the most speciose shrimp family within the infraorder Caridea, composed predominately of freshwater species and marine symbiotic species. The subject of this study is a clade of mainly free-living marine taxa representing a basally separated lineage from most of the symbiotic marine palaemonid genera. Phylogenetic and biogeographic relationships were explored by analysing sequence data from two mitochondrial and four nuclear markers. Maximum likelihood and Bayesian analyses, based on sequences from 52 species of 11 genera, provided similar tree topologies revealing the genera Palaemonella, Cuapetes and Eupontonia as non-monophyletic groups. Divergence time and S-DIVA analyses reveals that the focal clade originated during the Late Cretaceous in the Paleotethys region respective to the present Indo-West Pacific area, a minor part of which spread out to the eastern Pacific during the Paleocene, followed by further migration into the Atlantic (before the closure of the Panama Isthmus). The ancestral state reconstruction of host associations revealed eight independent symbiotic lineages originating from free-living ancestors, entering primary symbioses. The first associations with Cnidaria are estimated to have evolved in the Eocene. This study points to the need of taxonomic revisions of the non-monophyletic genera concerned.

Department of Biology and Ecology Faculty of Science University of Ostrava Chittussiho 10 710 00 Ostrava Czech Republic

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WoRMS Editorial Board. World Register of Marine Species. Retrieved 8 Mar 2022 from https://www.marinespecies.org at VLIZ (2022).

De Grave S, et al. A classification of living and fossil genera of decapod crustaceans. Raffles Bull. Zool. 2009;1:1–109.

De Grave S. Biogeography of Indo-Pacific Pontoniinae (Crustacea, Decapoda): A PAE analysis. J. Biogeogr. 2001;28:1239–1253. doi: 10.1046/j.1365-2699.2001.00633.x. DOI

Horká I, De Grave S, Fransen CHJM, Petrusek A, Duriš Z. Multiple host switching events shape the evolution of symbiotic palaemonid shrimps (Crustacea: Decapoda) Sci. Rep. 2016;6:e26486. doi: 10.1038/srep26486. PubMed DOI PMC

Chow LH, De Grave S, Tsang LM. Evolution of protective symbiosis in palaemonid shrimps (Decapoda: Caridea) with emphases on host spectrum and morphological adaptations. Mol. Phyl. Evol. 2021;162:107201. doi: 10.1016/j.ympev.2021.107201. PubMed DOI

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

Kou Q, et al. Phylogenetic relationships among genera of the Periclimenes complex (Crustacea: Decapoda: Pontoniinae) based on mitochondrial and nuclear DNA. Mol. Phyl. Evol. 2013;68:14–22. doi: 10.1016/j.ympev.2013.03.010. PubMed DOI

Gan Z, et al. Systematic status of the caridean families Gnathophyllidae Dana and Hymenoceridae Ortmann (Crustacea: Decapoda): A further examination based on molecular and morphological data. Chin. J. Oceanol. Limnol. 2015;33:149–158. doi: 10.1007/s00343-015-4007-z. DOI

De Grave S, Fransen CHJM, Page TJ. Let’s be pals again: major systematic changes in Palaemonidae (Crustacea: Decapoda) PeerJ. 2015;3:e1167. doi: 10.7717/peerj.1167. PubMed DOI PMC

Chow LH, De Grave S, Tsang LM. The family Anchistioididae Borradaile, 1915 (Decapoda: Caridea) is a synonym of Palaemonidae Rafinesque, 1815 based on molecular and morphological evidence. J. Crust. Biol. 2020;40:277–287. doi: 10.1093/jcbiol/ruaa012. DOI

Galil, B., Froglia, C. & Noel, P. CIESM atlas of exotic species in the Mediterranean. Vol. 2. Crustaceans: Decapods and stomatopods (ed. Briand, F.) 192 (CIESM Publishers, 2002).

Bruce AJ. Observation on the Indo-West-Pacific species of the genus Palaemonella Dana, 1852 (Decapoda, Pontoniinae) Crustaceana. 1970;19:273–287. doi: 10.1163/156854070X00365. DOI

Bruce AJ. A partial revision of the genus Periclimenes Costa, 1884 (Crustacea: Decapoda: Palaemonidae) Zootaxa. 2004;582:1–26. doi: 10.11646/zootaxa.582.1.1. DOI

Okuno J. Palaemonella shirakawai, a new species of shrimp (Crustacea: Decapoda: Palaemonidae), associated with burrow dwelling opistognathid fish from the Ryukyu Islands Japan. Zootaxa. 2017;4299:521–528. doi: 10.11646/zootaxa.4299.4.3. DOI

Anker A, De Grave S. Further records of burrow-associated palaemonid shrimps (Decapoda: Palaemonidae) Zootaxa. 2019;4612:145–150. doi: 10.11646/zootaxa.4612.1.13. PubMed DOI

Scotese CR, Scotese JD. Plate Tectonic Evolution of North America. PALEOMAP Project; 2006.

Cowman PF, Bellwood DR. Vicariance across major marine biogeographic barriers: temporal concordance and the relative intensity of hard versus soft barriers. Proc. R. Soc. Lond. B. 2013;280:e20131541. PubMed PMC

Bacon CD, et al. Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proc. Natl. Acad. Sci. U.S.A. 2015;112:6110–6115. doi: 10.1073/pnas.1423853112. PubMed DOI PMC

Montes C, et al. Middle Miocene closure of the Central American Seaway. Science. 2015;348:226–229. doi: 10.1126/science.aaa2815. PubMed DOI

O’Dea A, et al. Formation of the Isthmus of Panama. Sci. Adv. 2016;2:e1600883. doi: 10.1126/sciadv.1600883. PubMed DOI PMC

Fransen CHJM. The influence of land barriers on the evolution of Pontoniine Shrimps (Crustacea, Decapoda) living in association with molluscs and solitary ascidians. In: Renema W, editor. Biogeography, Time, and Place: Distributions, Barriers, and Islands. Springer; 2007. pp. 103–115.

Fransen CHJM. A review of information upon the coral hosts of commensal shrimps of the sub-family Pontoniinae Kingsley, 1878 (Crustacea, Decapoda, Palaemonidae) In: Mukundan C, Pillai CSG, editors. Proceedings of the Symposium on Corals and Coral Reefs. Mar. Biol. Assoc.; 1972. pp. 399–418.

Kou Q, Li XZ, Chan TY, Chu KH. Divergent evolutionary pathways and host shifts among the commensal pontoniine shrimps: A preliminary analysis based on selected Indo-Pacific species. Org. Divers. Evol. 2015;15:369–377. doi: 10.1007/s13127-014-0198-y. DOI

Bruce AJ. Notes on some Indo-Pacific Pontoniinae. XI. A re-examination of Philarius lophos Barnard, with the designation of a new genus. Ischnopontonia. Bull. Mar. Sci. 1966;16:584–598.

Bruce AJ. A synopsis of the Indo-West Pacific genera of the Pontoniinae (Crustacea: Decapoda: Pontoniinae) In: Fricke R, editor. Theses Zoologicae 25. Koeltz Scientific Books; 1995. pp. 1–172.

Ďuriš Z, Bruce AJ. A revision of the ‘petitthouarsii’ species-group of the genus Periclimenes Costa, 1844 (Crustacea: Decapoda: Palaemonidae) J. Nat. Hist. 1995;29:619–671. doi: 10.1080/00222939500770221. DOI

Marin I, Sinelnikov S. Partial redescription of pontoniine shrimps Cuapetes nilandensis (Borradaile, 1915) and Cuapetes seychellensis (Borradaile, 1915) (Decapoda: Palaemonidae: Pontoniinae) with remarks on taxonomic status of Cuapetes Clark, 1919 and Kemponia Bruce, 2004. Zootaxa. 2016;4173:557–568. doi: 10.11646/zootaxa.4173.6.3. PubMed DOI

Fransen CHJM, De Grave S. Evolution and radiation of shrimp-like decapods: an overview. In: Martin JW, Crandall A, Felder DL, editors. Decapod Crustacean Phylogenetics. CRC Press; 2009. pp. 257–272.

Kemp S. Notes on Crustacea Decapoda in the Indian Museum XV. Pontoniinae. Rec. Indian Mus. 1922;24:113–288.

Marin IN, Britayev TA. Symbiotic Community, Associated with Corals of the Genus Galaxea Oken, 1815 (Euphyllidae: Scleractinia) 148. KMK Scientific Press; 2014.

Bruce AJ. Vir colemani sp. nov., a new commensal pontoniine shrimp (Crustacea: Decapoda: Palaemonidae) from Papua New Guinea. In: Glasby CJ, editor. The Beagle, Records of the Northern Territory Museum of Arts and Sciences 19. Northern Territory Government; 2003. pp. 119–124.

Marin IN, Anker A. Two new species of the genus Vir Holthuis, 1952 from Vietnam (Crustacea: Decapoda: Palaemonidae) Arthropoda Sel. 2005;14:117–128.

Fransen CHJM, Holthuis LB. Vir smiti spec. nov., a new scleractinian associated pontoniine shrimp (Crustacea: Decapoda: Palaemonidae) from the Indo-West Pacific. Zool. Med. Leiden. 2007;81:101–114.

Bruce, A. J. Periclimenes kororensis n. sp., an unusual shrimp associate of the fungiid coral, Heliofungia actiniformis. Micronesica13, 33–43 (1977).

Bruce AJ. Eupontonia oahu sp. nov., a second species of the genus Eupontonia Bruce, 1971, (Crustacea: Decapoda: Pontoniinae) from Oahu Hawai’ian Islands. Zootaxa. 2010;2372:405–414. doi: 10.11646/zootaxa.2372.1.32. DOI

Bruce AJ. A report on some coral reef shrimps from the Philippine Islands. Asian Mar. Biol. 1989;6:173–192.

Ďuriš Z, Anker A. Athanas manticolus sp. nov., a new stomatopod-associated alpheid shrimp from Vietnam (Crustacea, Decapoda) Zootaxa. 2014;3784:550–558. doi: 10.11646/zootaxa.3784.5.4. PubMed DOI

Bambach RK. Phanerozoic biodiversity mass extinctions. Annu. Rev. Earth Planet. Sci. 2006;34:127–155. doi: 10.1146/annurev.earth.33.092203.122654. DOI

Wood R. Reef evolution. Oxford Univ; 1999.

Mindat.org (2022). Retrieved 21 Mar 2022 from https://www.mindat.org/

Fransen CHJM, Schubart CM, Moro L. A new species of Cuapetes (Decapoda, Caridea, Palaemonidae) from the Canary Islands. Crustaceana. 2022;95:353–371.

Titus BM, Daly M, Hamilton N, Berumen M, Baeza JA. Global species delimitation and phylogeography of the circumtropical “sexy shrimp” Thor amboinensis reveals a cryptic species complex and secondary contact in the Indo-West Pacific. J. Biogeogr. 2018;45:1275–1287. doi: 10.1111/jbi.13231. DOI

Shannon LV. The Benguela ecosystem. 1. Evolution of the Benguela, physical features and processes. In: Barnes M, Barnes H, editors. Oceanography and Marine Biology. An Annual Review 23. CRC Press; 1985. pp. 105–182.

Edgar RC. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Xia X. DAMBE6: New tools for microbial genomics, phylogenetics and molecular evolution. J. Hered. 2017;108:431–437. doi: 10.1093/jhered/esx033. PubMed DOI PMC

Xia XH, Xie Z, Salemi M, Chen L, Wang Y. An index of substitution saturation and its application. Mol. Phyl. Evol. 2003;26:1–7. doi: 10.1016/S1055-7903(02)00326-3. PubMed DOI

Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 2007;56:564–577. doi: 10.1080/10635150701472164. PubMed DOI

Vaidya G, Lohman DJ, Meier R. SequenceMatrix: Concatenation software for the fast assembly of multigene datasets with character set and codon information. Cladistics. 2011;27:171–180. doi: 10.1111/j.1096-0031.2010.00329.x. PubMed DOI

Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucl. Acids Res. 2016;44(W1):W232–W235. doi: 10.1093/nar/gkw256. PubMed DOI PMC

Minh BQ, Nguyen MAT, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 2013;30:1188–1195. doi: 10.1093/molbev/mst024. PubMed DOI PMC

Ronquist F, et al. Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

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) 1–8 (IEEE, 2010).

Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 2016;34:772–773. PubMed

Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. Tracer v1.6. (2014). Retrieved 21 Mar 2022 from http://tree.bio.ed.ac.uk/software/tracer/

Letunic I, Bork P. Interactive tree of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucl. Acids Res. 2021;49(W1):W293–W296. doi: 10.1093/nar/gkab301. PubMed DOI PMC

Bouckaert R, et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 2019;15:e1006650. doi: 10.1371/journal.pcbi.1006650. PubMed DOI PMC

Bouckaert R, Drummond A. bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evol. Biol. 2017;17:42. doi: 10.1186/s12862-017-0890-6. PubMed DOI PMC

Schubart CD, Diesel R, Hedges SB. Rapid evolution to terrestrial life in Jamaican crabs. Nature. 1998;393:363–365. doi: 10.1038/30724. DOI

Suchard MA, et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018;vey4:016. PubMed PMC

Rambaut, A. FigTree: Tree figure drawing tool version 1.4.3. (2016). Retrieved 21 Mar from http://tree.bio.ed.ac.uk/

Maddison, W. P. & Maddison, D. R. Mesquite: A Modular system for evolutionary analysis. Version 3.5. (2018). Retrieved 21 Mar 2022 from https://www.mesquiteproject.org/

Yu Y, Harris AJ, He XJ. S-DIVA (statistical dispersal-vicariance analysis): A tool for inferring biogeographic histories. Mol. Phyl. Evol. 2010;56:848–850. doi: 10.1016/j.ympev.2010.04.011. PubMed DOI

Yu Y, Harris AJ, Blair C, He XJ. RASP (reconstruct ancestral state in phylogenies): A tool for historical biogeography. Mol. Phyl. Evol. 2015;87:46–49. doi: 10.1016/j.ympev.2015.03.008. PubMed DOI

Scotese, C. R. PALEOMAP PaleoAtlas for GPlates and the PaleoData Plotter Program, PALEOMAP Project (2016). Retrieved 6 June from http://www.earthbyte.org/paleomap-paleoatlas-for-gplates/