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Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Integrative methods resolve taxonomy and relationships of snapping shrimps in the genus Synalpheus (Decapoda: Alpheidae) collected during the MNHN ‘Madibenthos’ expedition

Hossein Ashrafi https://orcid.org/0000-0003-1677-4775 A * and Kristin M. Hultgren https://orcid.org/0000-0002-5501-865X B
+ Author Affiliations
- Author Affiliations

A Department of Biology and Ecology, Faculty of Science, University of Ostrava, Chittussiho 10, CZ-71000 Ostrava, Czech Republic.

B Department of Biology, Seattle University, 901 12th Avenue, Seattle, WA 98122, USA.

* Correspondence to: ashrafi.hossein.s@gmail.com

Handling Editor: Shane Ahyong

Invertebrate Systematics 36(5) 389-418 https://doi.org/10.1071/IS21057
Submitted: 12 August 2021  Accepted: 8 January 2022   Published: 1 June 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

Extensive sampling around Martinique during the Muséum National d’Histoire Naturelle ‘Madibenthos’ expedition in 2016 resulted in a collection of hundreds of alpheid shrimps, of which 21 distinct species of Synalpheus Spence Bate, 1888 are studied herein. Combining results of a morphological analysis, a phylogenetic tree (combined 16S and COI) and species delimitation analyses (ABGD and PTP) indicates three species as new to science. These species are S. chaki sp. nov., S. corbariae sp. nov., and S. macdonaldi sp. nov. The first two new species belong to the S. rathbunae Coutière, 1909 species group, whereas the third new species broadly groups with the S. gambarelloides group. Additionally, 13 new country records of Synalpheus are reported for Martinique.

Keywords: Caribbean Sea, eusocial species, molecular phylogeny, new records, S. chaki, S. corbariae, S. macdonaldi, snapping shrimps, species delimitation, western Atlantic.


References

Anker, A, and De Grave, S (2016). An updated and annotated checklist of marine and brackish caridean shrimps of Singapore (Crustacea, Decapoda). The Raffles Bulletin of Zoology 34, 343–454.

Anker, A, and Tóth, E (2008). A preliminary revision of the Synalpheus paraneptunus Coutiere, 1909 species complex (Crustacea: Decapoda: Alpheidae). Zootaxa 1915, 1–28.
A preliminary revision of the Synalpheus paraneptunus Coutiere, 1909 species complex (Crustacea: Decapoda: Alpheidae).Crossref | GoogleScholarGoogle Scholar |

Anker, A, Pachelle, PP, De Grave, S, and Hultgren, KM (2012). Taxonomic and biological notes on some Atlantic species of the snapping shrimp genus Synalpheus Spence Bate, 1888 (Decapoda, Alpheidae). Zootaxa 3598, 1–96.
Taxonomic and biological notes on some Atlantic species of the snapping shrimp genus Synalpheus Spence Bate, 1888 (Decapoda, Alpheidae).Crossref | GoogleScholarGoogle Scholar |

Armstrong, JC (1949). New Caridea from the Dominican Republic. American Museum Novitates 1410, 1–22.

Aznar-Cormano, L, Brisset, J, Chan, TY, Corbari, L, Puillandre, N, Utge, J, Zbinden, M, Zuccon, D, and Samadi, S (2015). An improved taxonomic sampling is a necessary but not sufficient condition for resolving inter-families relationships in Caridean decapods. Genetica 143, 195–205.
An improved taxonomic sampling is a necessary but not sufficient condition for resolving inter-families relationships in Caridean decapods.Crossref | GoogleScholarGoogle Scholar | 25681232PubMed |

Baeza, JA, and Fuentes, MS (2013). Exploring phylogenetic informativeness and nuclear copies of mitochondrial DNA (numts) in three commonly used mitochondrial genes: mitochondrial phylogeny of peppermint, cleaner, and semi-terrestrial shrimps (Caridea: Lysmata, Exhippolysmata, and Merguia). Zoological Journal of the Linnean Society 168, 699–722.
Exploring phylogenetic informativeness and nuclear copies of mitochondrial DNA (numts) in three commonly used mitochondrial genes: mitochondrial phylogeny of peppermint, cleaner, and semi-terrestrial shrimps (Caridea: Lysmata, Exhippolysmata, and Merguia).Crossref | GoogleScholarGoogle Scholar |

Banner, AH, and Banner, DM (1964). Contributions to the knowledge of the alpheid shrimp of the Pacific Ocean, IX. Collections from the Phoenix and Line Islands. Pacific Science 18, 83–100.

Banner, DM, and Banner, AH (1972). Contributions to the knowledge of the alpheid shrimp of the Pacific Ocean. Crustaceana 23, 20–27.
Contributions to the knowledge of the alpheid shrimp of the Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Banner, DM, and Banner, AH (1975). The alpheid shrimp of Australia. Part 2: The genus Synalpheus. Records of the Australian Museum 29, 267–389.
The alpheid shrimp of Australia. Part 2: The genus Synalpheus.Crossref | GoogleScholarGoogle Scholar |

Banner, DM, and Banner, AH (1981). Annotated checklist of the alpheid shrimp of the Red Sea and Gulf of Aden. Zoölogische Verhandelingen 190, 1–99.

Banner, AH, and Banner, DM (1983). An annotated checklist of the alpheid shrimp from the western Indian ocean. Travaux et Documents de l’ORSTOM 158, 1–164.

Chace, FAJ (1972). The shrimps of the Smithsonian-Bredin Caribbean expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology 98, 1–179.
The shrimps of the Smithsonian-Bredin Caribbean expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia).Crossref | GoogleScholarGoogle Scholar |

Chace, FAJ (1988). The caridean shrimps (Crustacea: Decapoda) of the Albatross Philippine expedition, 1907–1910, part 5: family Alpheidae. Smithsonian Contributions to Zoology 466, 1–99.

Chak, ST, and Rubenstein, DR (2019). Social transitions in sponge-dwelling snapping shrimp. Current Opinion in Insect Science 34, 33–39.
Social transitions in sponge-dwelling snapping shrimp.Crossref | GoogleScholarGoogle Scholar | 31247415PubMed |

Chak, ST, Duffy, JE, Hultgren, KM, and Rubenstein, DR (2017). Evolutionary transitions towards eusociality in snapping shrimps. Nature Ecology & Evolution 1, 0096.
Evolutionary transitions towards eusociality in snapping shrimps.Crossref | GoogleScholarGoogle Scholar |

Christoffersen, ML (1979). Campagne de la Calypso au large des côtes Atlantiques de l’Amérique du Sud (1961–1962). I Decapod Crustacea: Alpheoida. Annales de l’Institut Océanographique 55, 297–377.

Coutière H (1905). Les Alpheidae. In ‘The fauna and geography of the Maldive and Laccadive archipelagoes, being the account of the work carried on and of the collections made by an expedition during the years 1899 and 1900’. (Ed. JS Gardiner) Vol. II, part IV, pp. 852–921, plates 870–887. (Cambridge University Press: Cambridge, UK)

Coutière, H (1909). The American species of snapping shrimps of the genus Synalpheus. Proceedings of the United States National Museum 36, 1–93.
The American species of snapping shrimps of the genus Synalpheus.Crossref | GoogleScholarGoogle Scholar |

Coutière, H (1910). The snapping shrimps (Alpheidae) of the Dry Tortugas, Florida. Proceedings of the United States National Museum 37, 485–487.
The snapping shrimps (Alpheidae) of the Dry Tortugas, Florida.Crossref | GoogleScholarGoogle Scholar |

Crandall, KA, and Fitzpatrick Jr, JF (1996). Crayfish molecular systematics: using a combination of procedures to estimate phylogeny. Systematic Biology 45, 1–26.
Crayfish molecular systematics: using a combination of procedures to estimate phylogeny.Crossref | GoogleScholarGoogle Scholar |

Dardeau, MR (1984). Synalpheus shrimps (Crustacea: Decapoda: Alpheidae). I. The Gambarelloides group, with a description of a new species. Memoirs of the Hourglass Cruises 7, 1–125.

Darriba, D, Taboada, GL, Doallo, R, and Posada, D (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 22847109PubMed |

De Grave, S, and Fransen, CHJM (2011). Carideorum catalogus: the recent species of the dendrobranchiate, stenopodidean, procarididean and caridean shrimps (Crustacea: Decapoda). Zoologische Mededelingen Leiden 85, 195–588.

De Man, JG (1910). Diagnoses of new species of macrurous decapod Crustacea from the «Siboga-Expedition». V. Tijdschrift der Nederlandsche Dierkundige Vereeniging 11, 287–319.

De Man, JG (1911). The Decapoda of the Siboga expedition, Part II, family Alpheidae. Sibogae Expedition 39a, 133–465.

Drummond, A, and Rambaut, A (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar | 17996036PubMed |

Duffy, JE (1996a). Eusociality in a coral-reef shrimp. Nature 381, 512–514.
Eusociality in a coral-reef shrimp.Crossref | GoogleScholarGoogle Scholar |

Duffy, JE (1996b). Synalpheus regalis, new species, a sponge-dwelling shrimp from the Belize Barrier Reef, with comments on host specificity in Synalpheus. Journal of Crustacean Biology 16, 564–573.
Synalpheus regalis, new species, a sponge-dwelling shrimp from the Belize Barrier Reef, with comments on host specificity in Synalpheus.Crossref | GoogleScholarGoogle Scholar |

Edgar, RC (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 15034147PubMed |

Geller, J, Meyer, C, Parker, M, and Hawk, H (2013). Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all‐taxa biotic surveys. Molecular Ecology Resources 13, 851–861.
Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all‐taxa biotic surveys.Crossref | GoogleScholarGoogle Scholar | 23848937PubMed |

Herrick, FH (1891). Alpheus: a study in the development of Crustacea. In ‘The embryology and metamorphosis of the Macrura’. (Eds WK Brooks, FH Herrick) Memoirs of the National Academy of Sciences, Washington 5, 370–463.

Hermoso-Salazar, M, Wicksten, M, and Morrone, JJ (2008). Phylogenetic analysis of the Paulsoni species group (Decapoda: Alpheidae) from the American Pacific, with implications for the phylogenetic classification of the genus Synalpheus. Zootaxa 1744, 19–30.
Phylogenetic analysis of the Paulsoni species group (Decapoda: Alpheidae) from the American Pacific, with implications for the phylogenetic classification of the genus Synalpheus.Crossref | GoogleScholarGoogle Scholar |

Holthuis, LB (1958). Contributions to the knowledge of the Red Sea. nos. 8–9. Crustacea Decapoda from the Northern Red Sea (Gulf of Aqaba and Sinai peninsula). I. Macrura. Bulletin of the Sea Fisheries Research Station, Haifa 17, 1–40.

Hultgren, KM, and Brandt, A (2015). Taxonomy and phylogenetics of the Synalpheus paraneptunus species-complex (Decapoda: Alpheidae), with a description of two new species. Journal of Crustacean Biology 35, 547–558.
Taxonomy and phylogenetics of the Synalpheus paraneptunus species-complex (Decapoda: Alpheidae), with a description of two new species.Crossref | GoogleScholarGoogle Scholar |

Hultgren, KM, and Duffy, JE (2011). Multi-locus phylogeny of sponge-dwelling snapping shrimp (Caridea: Alpheidae: Synalpheus) supports morphology-based species concepts. Journal of Crustacean Biology 31, 352–360.
Multi-locus phylogeny of sponge-dwelling snapping shrimp (Caridea: Alpheidae: Synalpheus) supports morphology-based species concepts.Crossref | GoogleScholarGoogle Scholar |

Hultgren, KM, Macdonald, KS, and Duffy, JE (2010). Sponge-dwelling snapping shrimps of Curaçao, with descriptions of three new species. Zootaxa 2372, 221–262.
Sponge-dwelling snapping shrimps of Curaçao, with descriptions of three new species.Crossref | GoogleScholarGoogle Scholar |

Hultgren, KM, Macdonald, KS, and Duffy, JE (2011). Sponge-dwelling snapping shrimps (Alpheidae: Synalpheus) of Barbados, West Indies, with a description of a new eusocial species. Zootaxa 2834, 1–16.
Sponge-dwelling snapping shrimps (Alpheidae: Synalpheus) of Barbados, West Indies, with a description of a new eusocial species.Crossref | GoogleScholarGoogle Scholar |

Hultgren, KM, Hurt, C, and Anker, A (2014). Phylogenetic relationships within the snapping shrimp genus Synalpheus (Decapoda: Alpheidae). Molecular Phylogenetics and Evolution 77, 116–125.
Phylogenetic relationships within the snapping shrimp genus Synalpheus (Decapoda: Alpheidae).Crossref | GoogleScholarGoogle Scholar | 24680914PubMed |

Lefébure, T, Douady, CJ, Gouy, M, and Gibert, J (2006). Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution 40, 435–447.
Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation.Crossref | GoogleScholarGoogle Scholar | 16647275PubMed |

Macdonald, KS, and Duffy, JE (2006). Two new species of sponge-dwelling snapping shrimp from the Belizean Barrier Reef, with a synopsis of the Synalpheus brooksi species complex. American Museum Novitates 3543, 1–22.
Two new species of sponge-dwelling snapping shrimp from the Belizean Barrier Reef, with a synopsis of the Synalpheus brooksi species complex.Crossref | GoogleScholarGoogle Scholar |

Macdonald, KS, Hultgren, KM, and Duffy, JE (2009). The sponge-dwelling snapping shrimps (Crustacea, Decapoda, Alpheidae, Synalpheus) of Discovery Bay, Jamaica, with descriptions of four new species. Zootaxa 2199, 1–57.
The sponge-dwelling snapping shrimps (Crustacea, Decapoda, Alpheidae, Synalpheus) of Discovery Bay, Jamaica, with descriptions of four new species.Crossref | GoogleScholarGoogle Scholar |

Matzen da Silva , J, Creer , S, dos Santos , A, Costa , AC, Cunha , MR, Costa , FO, and Carvalho , GR (2011). Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca). PLoS One 6, e19449–e19449.
Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca).Crossref | GoogleScholarGoogle Scholar | 21589909PubMed |

Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE)’, 14 November 2010, New Orleans, LA, USA. INSPEC Accession Number 11705685. (IEEE)
| Crossref |

Morrison, CL, Rios, R, and Duffy, JE (2004). Phylogenetic evidence for an ancient rapid radiation of Caribbean sponge-dwelling snapping shrimps (Synalpheus). Molecular Phylogenetics and Evolution 30, 563–581.
Phylogenetic evidence for an ancient rapid radiation of Caribbean sponge-dwelling snapping shrimps (Synalpheus).Crossref | GoogleScholarGoogle Scholar | 15012939PubMed |

Nylander, J, Ronquist, F, Huelsenbeck, J, and Nieves-Aldrey, J (2004). Bayesian phylogenetic analysis of combined data. Systematic Biology 53, 47–67.
Bayesian phylogenetic analysis of combined data.Crossref | GoogleScholarGoogle Scholar | 14965900PubMed |

Palumbi SR, Martin A, Romano S, Mcmillan WO, Stice L, Grabowski G (1991) ‘The simple fool’s guide to PCR, version 2.0.’ (University of Hawaii Press: Honolulu, HI, USA)

Pequegnat, LH, and Heard, RW (1979). Synalpheus agelas, new species of snapping shrimp from the Gulf of Mexico and Bahama Islands (Decapoda: Caridea: Alpheidae). Bulletin of Marine Science 29, 110–116.

Puillandre, N, Lambert, A, Brouillet, S, and Achaz, G (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 21883587PubMed |

Rambaut, A, Drummond, AJ, Xie, D, Baele, G, and Suchard, MA (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901.
Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |

Ríos, R, and Duffy, JE (1999). Description of Synalpheus williamsi, a new species of sponge-dwelling shrimp (Crustacea: Decapoda: Alpheidae), with remarks on its first larval stage. Proceedings of the Biological Society of Washington 112, 541–552.

Ríos, R, and Duffy, JE (2007). A review of the sponge-dwelling snapping shrimp from Carrie Bow Cay, Belize, with description of Zuzalpheus, new genus, and six new species. Zootaxa 1602, 1–89.
A review of the sponge-dwelling snapping shrimp from Carrie Bow Cay, Belize, with description of Zuzalpheus, new genus, and six new species.Crossref | GoogleScholarGoogle Scholar |

Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Hohna, S, Larget, B, Liu, L, Suchard, MA, and Huelsenbeck, JP (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |

Stecher, G, Tamura, K, and Kumar, S (2020). Molecular evolutionary genetics analysis (MEGA) for macOS. Molecular Biology and Evolution 37, 1237–1239.
Molecular evolutionary genetics analysis (MEGA) for macOS.Crossref | GoogleScholarGoogle Scholar | 31904846PubMed |

Zhang, J, Kapli, P, Pavlidis, P, and Stamatakis, A (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.
A general species delimitation method with applications to phylogenetic placements.Crossref | GoogleScholarGoogle Scholar | 23990417PubMed |