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Are there true cosmopolitan sipunculan worms? A genetic variation study within Phascolosoma perlucens (Sipuncula, Phascolosomatidae)

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Abstract

Phascolosoma perlucens is one of the most common intertidal sipunculan species and has been considered a circumtropical cosmopolitan taxon due to the presence of a long-lived larva. To verify whether P. perlucens is a true cosmopolitan species or a complex of cryptic forms, we examined the population structure and demographics of 56 putative P. perlucens individuals from 13 localities throughout the tropics. Analysis of two mitochondrial markers, cytochrome c oxidase subunit I and 16S rRNA, suggests high levels of genetic differentiation between distantly located populations of P. perlucens. At least four different lineages identified morphologically as P. perlucens were distinguished. These lineages are likewise supported by phylogenetic analysis of the two mitochondrial markers and by the haplotype network analysis. Our results suggest that P. perlucens is a case of overconservative taxonomy, rejecting the alleged cosmopolitanism of P. perlucens. However, cryptic speciation also exists in some areas, including a possible case of geminate species across the Isthmus of Panama.

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Acknowledgments

This study is dedicated to the memory of Edward Cutler who guided us through the study of sipunculans. We will always remember his friendship and passion for his beloved sipunculan worms. Anja Schulze, Harlan Dean, Joergensen Hylleberg, Mary Rice, and Ramlall Biseswar assisted with samples, and Cláudio Gonçalves Tiago with fieldwork in New Caledonia. Sónia Andrade assisted with population genetics software, and Prashant Sharma with phylogenetic analyses. This study was funded by a grant from the MarCraig foundation, which supported Gisele Kawauchi and the sipunculan research at the Giribet Laboratory. Fieldwork to New Caledonia was supported by the Putnam Expedition Grants program of the Museum of Comparative Zoology. David Paulaud from Direction de l’Environnement (Province Sud) facilitated collecting permits for New Caledonia. Bertrand Richer De Forges, Jean-Lou Justine, and Claire Goiran (IRD-Noumea) assisted with logistics in Noumea. Ann Covert and the Museum of Comparative Zoology provided additional funding and support. Three anonymous reviewers and Associate Editor Cynthia Riginos provided comments that helped to improve earlier versions of this manuscript.

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  1. Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA

    Gisele Y. Kawauchi & Gonzalo Giribet

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  1. Gisele Y. Kawauchi
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Correspondence to Gisele Y. Kawauchi.

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Communicated by C. Riginos.

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Appendices

Appendix 1

Voucher details for specimens used in the molecular analyses. Repositories abbreviated as follows: Museum of Comparative Zoology, Harvard University (MCZ)

Apiosoma misakianum (Ikeda 1904)

MCZ DNA100737. Israel: Eilat; on old rope; 15-30 m; October 2002; leg. N. Ben Eliahu; determined by A. Schulze

Aspidosiphon laevis de Quatrefages, 1865

MCZ DNA102616. New Caledonia: Ilot Maitre, South Province; in coral rubble; 6 m deep; 22°19′35.9″S 166°24′40.2″E; G. Kawauchi satation NC03; 16 November 2007; leg. G. Kawauchi, C. Tiago; determined by G. Kawauchi

Antillesoma antillarum (Grübe and Oersted, 1858)

MCZ DNA100759. Barbados: Six Men’s Bay; 27 June 2002; leg. E.B. Cutler, G. Kawauchi, J. Saiz-Salinas, A. Schulze; determined by A. Schulze

Phascolosoma granulatum (Leuckart 1828)

MCZ DNA100201. Spain: Girona, Blanes; 12 August 1997; leg. G. Giribet, C. Palacín; determined by E.B. Cutler and H.K. Dean

Phascolosoma nigrescens (Keferstein 1865)

MCZ DNA100822. South Africa: KwaZulu Natal, St. Lucia, Perrier’s Rock; under oyster shells (Saccostrea cucculata); 18 October 2002; leg. R. Biseswar; determined by A. Schulze

Phascolosoma turnerae Rice 1985

MCZ DNA100230. Bahamas: Southwest Reef; in artificial fibrous collector, deployed on sandy bottom at 519 m deep; approximately 24°52.88′N 77° 32.23′W; Rice station 324Q; February 2000; Harbor Branch Johnson Sea Link Submersible, Dive 3197; determined by M. Rice

Phascolosoma scolops (Selenka and Man 1883)

MCZ DNA100814. South Africa: KwaZulu Natal, St. Lucia, Park Rynie Beach; intertidal; 22 August 2002; leg. R. Biseswar; determined by A. Schulze

Phascolosoma stephensoni (Stephen 1942)

MCZ DNA100818. South Africa: KwaZulu Natal, St. Lucia, Park Rynie Beach; intertidal; 9 September 2002; leg. R. Biseswar; determined by A. Schulze

Phascolosoma albolineatum (Baird 1868)

MCZ DNA100396. Thailand: Phuket; intertidal reef; February 2001; leg. J. Hylleberg; determined by E.B. Cutler and H.K. Dean

Phascolosoma perlucens Baird 1868

MCZ DNA100748. Barbados: Bank Reef; in coral rubble; 15–20 m deep; 26 June 2002; leg. G. Kawauchi, J. Saiz-Salinas, A. Schulze; determined by A. Schulze

MCZ DNA100749. Barbados: Bank Reef; in coral rubble; 15–20 m deep; 24 June 2002; leg. G. Kawauchi, J. Saiz-Salinas, A. Schulze; determined by A. Schulze

MCZ DNA100750. Barbados: Martin’s Bay; in coral rubble; 21 June 2002; leg. E.B. Cutler, G. Kawauchi, J. Saiz-Salinas, A. Schulze; determined by A. Schulze

MCZ DNA100751. Barbados: River Bay; 15–20 m deep; 26 June 2002; leg. G. Kawauchi, J. Saiz-Salinas, A. Schulze; determined by A. Schulze

MCZ DNA100995. Belize: north of Southwater Caye, Tabacco Reef; intertidal rock; M. Rice station CB03-10E; 20 April 2003; leg. M. Rice, A. Schulze; determined by M. Rice and A. Schulze

MCZ DNA101914 (MCZ IZ66181). Venezuela: Cubagua Island; 10°48′14.7″N 64°9′53.76″W; 16 December 2003; I. leg. Hernández-Ávila; determined by H.K. Dean

MCZ DNA101915 (MCZ IZ66188). Venezuela: Cubagua Island; in rocks; Thalassia bed; 10°48′7,68″N 64°10′52″W; 15 January 2004; leg. I. Hernández-Ávila; determined by H.K. Dean

MCZ DNA103542. USA: Florida, Florida Keys, Missouri Key; in coralline limestone; intertidal; 24°40.6′N 81°09.9″W; M. Rice station 170j; 6 April 2008; leg. A. Maiorova; determined by M. Rice

MCZ DNA103543. USA: Florida, Lake Worth, Peanut Island; on sea wall at boat launch, among clumps of encrusting vermetids, oysters, and barnacles; 26°47.0′N 80°02.5′ W; M. Rice station 218c; 30 April 2008; leg. A. Shulze; determined by M. Rice

MCZ DNA103802. Costa Rica: Bahía Salinas, Isla Bolaños, rocky intertidal, 16 August 2006, leg. H.K. Dean, determined by H.K. Dean

MCZ DNA101013. USA: Florida, St. Lucie Inlet, Bessy Cove, on sea wall and rocks, among vermetid and oyster encrustations; 27°11.1′N 80°09.9′W; M. Rice station 156jj; 10 March 2008; leg. S. Reed; determined by M. Rice

Phascolosoma aff. perlucens

MCZ DNA100395. Thailand: Phuket; intertidal reef; February 2000; leg. J. Hylleberg; determined by E.B. Cutler and H.K. Dean

MCZ DNA100819. South Africa: KwaZulu Natal, St. Lucia, Perrier’s Rock; under oyster shells (Saccostrea cucculata); intertidal; 10 October 2002; leg. R. Biseswar; determined by A. Schulze

MCZ DNA100820. South Africa: KwaZulu Natal, St. Lucia, Park Rynie Beach; intertidal; 22 August 2002; leg. R. Biseswar; determined by A. Schulze

MCZ DNA100821. South Africa: KwaZulu Natal, St. Lucia, Park Rynie Beach; intertidal; 9 September 2002; leg. R. Biseswar; determined by A. Schulze

MCZ DNA102620. New Caledonia: South Province, Ilot Maitre; in coral rubble; 6 m deep; 22°19′35.9”S 166°24′40.2″E; G. Kawauchi station NC03; 16 November 2007; leg. G. Kawauchi, C. Tiago; determined by G. Kawauchi

Appendix 2

List of slides with hooks deposited at the MCZ

Species name

MCZ accession number

Phascolosoma aff. perlucens

DNA100395

Phascolosoma aff. perlucens

DNA100395-6

Phascolosoma aff. perlucens

DNA100395-8

Phascolosoma aff. perlucens

DNA100395-9

Phascolosoma albolineatum

DNA100396-2

Phascolosoma perlucens

DNA100748

Phascolosoma perlucens

DNA100748-5

Phascolosoma aff. perlucens

DNA100819-7

Phascolosoma aff. perlucens

DNA100819-9

Phascolosoma aff. perlucens

DNA100820

Phascolosoma aff. perlucens

DNA100820-4

Phascolosoma aff. perlucens

DNA100820-8

Phascolosoma aff. perlucens

DNA100821

Phascolosoma perlucens

DNA100995-3

Phascolosoma perlucens

DNA101013

Phascolosoma perlucens

DNA101914

Phascolosoma perlucens

DNA103542-2

Phascolosoma perlucens

DNA103543-1

Phascolosoma perlucens

DNA103802-2

Phascolosoma aff. perlucens

DNA102620-1

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Kawauchi, G.Y., Giribet, G. Are there true cosmopolitan sipunculan worms? A genetic variation study within Phascolosoma perlucens (Sipuncula, Phascolosomatidae). Mar Biol 157, 1417–1431 (2010). https://doi.org/10.1007/s00227-010-1402-z

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