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(Sipuncula: Antillesomatidae), with the Description of a New Species Morphological and molecular differences between the Amphiamerican populations of Antillesoma (Sipuncula: Antillesomatidae), with the description of a new species Itzahí Silva-Morales1, Mónica J. López-Aquino2, Valentina Islas-Villanueva2, Fernando Ruiz-Escobar1 & J. Rolando Bastida-Zavala1 1. Laboratorio de Sistemática de Invertebrados Marinos (LABSIM), Universidad del Mar, campus Puerto Ángel, Oaxaca, 70902, México, [email protected] 2. Laboratorio de Genética y Microbiología, Universidad del Mar, campus Puerto Ángel, Oaxaca, 70902, México. Received 29-XI-2018. Corrected 18-V-2019. Accepted 30-VI-2019. ABSTRACT. Introduction: The sipunculans are a group of marine invertebrates that have been little stud- ied in the tropical eastern Pacific (TEP). Antillesoma antillarum is a species belonging to the monospecific family Antillesomatidae, considered widely distributed in tropical and subtropical localities across the globe. Objective: The main objective of this work was to examine the morphological and molecular differences between specimens from both coasts of tropical America to clarify the taxonomy of this species. Methods: We examined the morphology with material from the Mexican Caribbean and southern Mexican Pacific. To perform molecular analyses, two sequences of the COI molecular marker were obtained from specimens col- lected in Panteón Beach, Oaxaca, southern Mexican Pacific, and compared with four sequences identified as A. antillarum in GenBank, all of them from different localities. A phylogenetic reconstruction was performed with the maximum likelihood method and genetic distances were calculated with the Kimura 2P model and com- pared to reference values. Results: The phylogenetic analysis revealed three different lineages of Antillesoma that are well supported by bootstrap values: Antillesoma antillarum sensu stricto from the Caribbean Sea and Florida; a sister group to the one represented by our samples from the Mexican Pacific; and a third group from Thailand. Conclusion: Based on morphological traits and molecular data, Antillesoma mexicanum sp. nov. is described from the Mexican Pacific, differing from A. antillarum in the trunk papillae, color patterns and, addi- tionally, the specimens from the Caribbean attain significantly bigger trunk sizes than the ones Pacific. Key words: COI, cryptic species, genetic distances, sipunculans. Silva-Morales, I., López-Aquino, M. J., Islas-Villanueva, V., Ruiz-Escobar, F., & Bastida-Zavala, J. R. (2019). Morphological and molecular differences between the Amphiamerican populations of Antillesoma (Sipuncula: Antillesomatidae), with the description of a new species. Revista de Biología Tropical, 67(S5) Suplemento, S101-S109. The Sipuncula is a small group of unseg- bodies when contracted (Cutler, 1994). Recent mented vermiform protostomes (Murina, 1984; phylogenetic hypotheses have suggested their Cutler, 1994). Their most noticeable feature placement within Annelida, based entirely on is a body divided into a retractable introvert molecular analyses (Staton, 2003; Struck et al., and trunk, and they are commonly known as 2007; Dordel, Fisse, Purschke, & Struck, 2010; “peanut worms”, owing to the shape of their Lemer et al., 2016), although this proposal Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(S5) Supplement: S101-S109, July 2019 101 conflicts with the traditional definitions of both populations of Antillesoma are calculated and taxa (Boyle & Rice, 2018) and has not yet been compared to reference values in other genera. fully accepted (Saiz, 2018). Finally, a new species of Antillesoma from the Gibbs & Cutler (1987) proposed a taxo- Mexican Pacific is described. nomic classification based on their previous morphology-based phylogenetic analysis (Cut- MATERIAL AND METHODS ler & Gibbs, 1985). Kawauchi, Sharma, & Giribet (2012) conducted a multi-gene phy- Specimens regarded as A. antillarum were logenetic analysis, which required the erec- revised in two collections: Colección Científica tion of two new families (Siphonosomatidae de Invertebrados Marinos (OAX-CC-249-11) and Antillesomatidae) and the synonymy of at Laboratorio de Sistemática de Invertebrados Themistidae and Phascolionidae with Golfingi- Marinos (LABSIM), Universidad del Mar, and idae. This classification was reevaluated using the Colección de Referencia del Bentos Costero transcriptomics by Lemer et al. (2016), but has (ECO-CH-B) at El Colegio de la Frontera Sur not yet replaced the traditional classification of (ECOSUR, Chetumal). The external anatomy Gibbs & Cutler (1987) on the World Sipuncula was analyzed with the aid of a Carl Zeiss Database (Saiz, 2018). stereomicroscope, and some specimens were To date, the family Antillesomatidae con- dissected in order to describe internal traits, tains a single species, Antillesoma antillarum using the identification key of Cutler (1994). A (Grube & Öersted in Grube, 1858). The type t-Student test was used to compare mean size locality of this species is Puntarenas, Costa of the trunk between the specimens from the Rica and Saint Croix, Virgin Islands (Grube, Caribbean and Pacific. 1858). As the type material was not clearly Specimens were extracted from coral rub- established, Cutler & Cutler (1983) revised ble from the intertidal zone of Panteón Beach, material from different tropical and subtropical Puerto Ángel, Oaxaca (15°39’49” N, 96°29’39” localities, obtaining a long list of synonyms, W), and retractor muscles were isolated in redescribing the species based on material accordance with Kawauchi & Giribet (2010). from Barbados and Saint Croix, and conclud- The tissues were fixed in 96% ethanol and total ing that A. antillarum is widely distributed in DNA was extracted from two specimens using the coastal zones of tropical and subtropical the Animal and Fungi DNA Preparation Kit of localities of the world. Unfortunately, the new Jena Bioscience (Jena, Germany), following type locality was also not specified (Cutler & the instructions of the manufacturer. The cyto- Cutler, 1983: 183). chrome oxidase subunit I (COI) was amplified Some relatively recent works on Sipun- in polymerase chain reaction (PCR) using the cula used molecular tools to solve problems primers LCO1490-HCO2198 (Folmer, Black, of taxonomic identification where morphol- Hoeh, Lutz, & Vrijenhoek, 1994). The 15 μl ogy offered limited resolution (Staton & Rice, PCR reaction volumes were composed of 9.4 1999; Kawauchi & Giribet, 2010; Schulze, μl distilled water, 3 μl buffer [5x], 0.1 μl MgCl Maiorova, Timm, & Rice, 2012; Kawauchi & [50 mM], 0.1 μl Taq [5 μ/μl], 0.2 of each primer Giribet, 2014; Johnson, Sanders, Maiorova, (100 pM), and 2 μl DNA. Thermal cycling con- & Schulze, 2016). The wide distribution of sisted in an initial denaturing at 94 °C (5 min), several species (see Cutler 1994) has been followed by 35 cycles of 94 °C (45 s), 46 °C questioned by these studies. Therefore, the (45 s) and 72 °C (45 s), with a final extension objective of this study is to demonstrate the at 72 °C (7 min). PCR products were viewed in differences between the amphiamerican popu- a 1 % agarose gel. DNA extraction and Sanger lations of Antillesoma by means of the analysis sequencing were performed at the Laborato- of molecular and morphological characters. rio Nacional de Biodiversidad (LANABIO), In this work, the genetic distances among Instituto de Biología, UNAM. Sequences were 102 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(S5) Supplement: S101-S109, July 2019 edited with Geneious Pro v. 5.1.7 (Biomatters Ltd., New Zealand), checking for ambiguities and reading errors. GenBank accession num- bers for our new sequences are MK036430 and MK036431. Four A. antillarum sequences were retrieved from GenBank and added to our data- set, three of them from the Western Atlantic (accession numbers: DQ300102, AY161134, GU230172) and the fourth from the Indo- Pacific (accession number: JN865120). Phas- colosoma perlucens Baird, 1868 (accession number: GU190304) was included as an out- group based on previous analyses. Sequences were aligned manually in Bioedit v. 7 (Hall, 1999). Maximum Likelihood phylogenetic reconstruction was performed under the Gen- Fig. 1. Maximum-likelihood phylogenetic tree under the GTR model obtained in PhyML 3.0, with a bootstrap eral Time-Reversible (GTR) model as sug- of 1 000 replicates and Phascolosoma perlucens as the gested by PhyML 3.0 (Guindon et al. 2010), outgroup. following the Akaike Information Criterion. Genetic distances were calculated among the Morphological analyses: Specimens of A. Antillesoma lineages in MEGA7.0.26 (Kumar, antillarum from the southern Mexican Pacific Stecher, & Tamura, 2016) with the Kimura (Fig. 2A-B) and from the Mexican Carib- two-Parameter (Kimura-2P). For comparison, bean (Fig. 2C-D) are different in the trunk size genetic distances were calculated between P. (t-student test, p < 0.01). The average in the perlucens, Phascolosoma agassizii Keferstein, Mexican Pacific population is 7 mm (n= 40, 1866 and Sipunculus nudus Linnaeus, 1766, r= 2-15 mm, µ= 6.90, SD= 1.03), while in the made available by Kawauchi & Giribet (2010), Mexican Caribbean it is 18 mm (n= 51, r= 9-32 Schulze et al. (2012) and Kawauchi & Giribet mm, µ= 18.01, SD= 5.90). (2014), respectively. SYSTEMATIC ACCOUNT RESULTS Phylum Sipuncula Rafinesque, 1884 Molecular analyses: The dataset, includ- Family Antillesomatidae Kawauchi, ing our two new COI sequences, had an Sharma & Giribet, 2012 alignment length of 541 bp. The six analyzed Genus
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