Hostname: page-component-6bf8c574d5-vmclg Total loading time: 0 Render date: 2025-02-17T18:35:24.566Z Has data issue: false hasContentIssue false
  • English
  • Français

Population structure of the fireworm Hermodice carunculata in the wider Caribbean, Atlantic and Mediterranean Sea

Published online by Cambridge University Press:  08 February 2023

Mariel A. Cruz Ramos  and
Nikolaos V. Schizas Open the ORCID record for Nikolaos V. Schizas [Opens in a new window]
Mariel A. Cruz Ramos
Affiliation:
Department of Marine Sciences, University of Puerto Rico at Mayagüez, Call Box 9000, Mayagüez, PR 00681, USA
Nikolaos V. Schizas*
Affiliation:
Department of Marine Sciences, University of Puerto Rico at Mayagüez, Call Box 9000, Mayagüez, PR 00681, USA
*
Author for correspondence: Nikolaos V. Schizas, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The bearded fireworm Hermodice carunculata is a conspicuous omnivorous benthic invertebrate distributed in the wider Atlantic Ocean, Mediterranean Sea and the Red Sea. Questions were raised in the past regarding the taxonomic status of amphiatlantic fireworm specimens but subsequent analysis of morphological data with new molecular data reconfirmed the presence of only one species, H. carunculata with amphiatlantic distribution. Hermodice carunculata has been the subject of several taxonomic and genetic studies but there are still questions regarding the genetic diversity and population structure of the species throughout its range. We contributed to the genetic studies of H. carunculata with ~200 new samples from over 20 locations in the Caribbean, Eastern Atlantic Ocean and the Mediterranean Sea. We sequenced the mitochondrial markers Cytochrome c oxidase Subunit I (COI) and Cytochrome b (Cytb) from each polychaete to examine the patterns of genetic diversity of H. carunculata. Our data revealed a significant population structure between the Caribbean H. carunculata including those from Brazil compared with those from the eastern Atlantic (Tenerife, Canary Islands) and eastern Mediterranean (Greece and Malta). We inferred rates of gene flow between eastern and western Atlantic populations by estimating the bidirectional effective migration rate (Nem). We corroborate previous studies indicating the existence of one species with genetically distinct populations. However, the biological significance of the observed population divergence should be evaluated with cross-breeding experiments.

Keywords

Amphiatlantic distributionCOICytbgenetic diversitypolychaetepopulation subdivisionPuerto Rico
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 103 , 2023 , e14
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Current Address: University of Guam, Marine Laboratory, 303 University Drive UOG Station, Mangilao, GU 96923, USA

References

Ahrens, JB, Borda, E, Barroso, R, Paiva, PC, Campbell, AM, Wolf, A, Nugues, MM, Rouse, GW and Schulze, A (2013) The curious case of Hermodice carunculata (Annelida: Amphinomidae): evidence for genetic homogeneity throughout the Atlantic Ocean and adjacent basins. Molecular Ecology 22, 2280–2291.CrossRefGoogle ScholarPubMed
Andras, PJ, Rypien, KL and Harvell, CD (2013) Range-wide population genetic structure of the Caribbean Sea fan coral, Gorgonia ventalina. Molecular Ecology 22, 56–73.CrossRefGoogle ScholarPubMed
Baird, W (1870) Remarks on several genera of annelids, belonging to the group Eunicea, with a notice of such species as are contained in the collection of the British Museum, and a description of some others hitherto undescribed. Journal of the Linnean Society of London 10, 341–361.CrossRefGoogle Scholar
Bandelt, H, Forster, P and Röhl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Barnes, DKA (2002) Invasions by marine life on plastic debris. Nature 416, 808–809.CrossRefGoogle ScholarPubMed
Barroso, R, Almeida, D, Contins, M, Filgueiras, D and Dias, R (2016) Hermodice carunculata (Pallas, 1766) (Polychaeta: Amphinomidae) preying on starfishes. Marine Biodiversity 46, 333–334.CrossRefGoogle Scholar
Barroso, R, Filgueiras, D, Contins, M and Kudenov, J (2017) First report of the fireworm Hermodice carunculata (Annelida: Amphinomidae) preying on a sea cucumber. International Journal of Aquatic Biology 5, 282–285.Google Scholar
Barroso, R, Klautau, M, Solé-Cava, AM and Paiva, PC (2009) Eurythoe complanata (Polychaeta: Amphinomidae), the ‘cosmopolitan’ fireworm, consists of at least three cryptic species. Marine Biology 157, 69–80.CrossRefGoogle Scholar
Baums, IB, Miller, MW and Hellberg, ME (2006) Geographic variation in clonal structure in a reef building Caribbean coral, Acropora palmata. Ecological Monographs 76, 503–519.CrossRefGoogle Scholar
Beerli, P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22, 341–345.CrossRefGoogle ScholarPubMed
Beerli, P and Felsenstein, J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152, 763–773.CrossRefGoogle ScholarPubMed
Beerli, P, Mashayekhi, S, Sadeghi, M, Khodaei, M and Shaw, K (2019) Population genetic inference with MIGRATE. Current Protocols in Bioinformatics 68, e87.CrossRefGoogle ScholarPubMed
Beltran, DR, Schizas, NV, Appeldoorn, RS and Prada, C (2017) Effective dispersal of a Caribbean reef fish is smaller than current spacing among marine protected areas. Nature Scientific Reports 7, 4689.CrossRefGoogle ScholarPubMed
Breton, S, Dufresne, F, Desrosiers, G and Blier, PU (2003) Population structure of two northern hemisphere polychaetes, Neanthes virens and Hediste diversicolor (Nereididae), with different life-history traits. Marine Biology 142, 707–715.CrossRefGoogle Scholar
Briggs, JC (1974) Marine Zoogeography. New York, NY: MacGraw-Hill.Google Scholar
Carlon, DB and Budd, AF (2002) Incipient speciation across a depth gradient in a scleractinian coral? Evolution 56, 2227–2242.Google Scholar
Chatzigeorgiou, G, Sarropoulou, E, Vasileiadou, K, Brown, C, Faulwetter, S, Kotoulas, G and Arvanitidis, CD (2014) Community structure and population genetics of Eastern Mediterranean polychaetes. Frontiers in Marine Science 1, 1–8.CrossRefGoogle Scholar
Chu, KH, Tam, PF, Fung, CH and Chen, QC (1997) A biological survey of ballast water in container ships entering Hong Kong. Hydrobiologia 352, 201–206.CrossRefGoogle Scholar
Crawford, DC, Carlson, CS, Rieder, MJ, Carrington, DP, Yi, Q, Smith, JD, Eberle, MA, Kruglyak, L and Nickerson, DA (2004) Haplotype diversity across 100 candidate genes for inflammation, lipid metabolism, and blood pressure regulation in two populations. American Journal of Human Genetics 74, 610–622.CrossRefGoogle ScholarPubMed
Darriba, D, Posada, D, Kozlov, AM, Stamatakis, A, Morel, B and Flouri, T (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37, 291–294.CrossRefGoogle ScholarPubMed
Dasmahapatra, KK, Elias, M, Hill, RI, Hoffman, JI and Mallet, J (2010) Mitochondrial DNA barcoding detects some species that are real, and some that are not. Molecular Ecology Resources 10, 264–273.CrossRefGoogle ScholarPubMed
De Queiroz, K (2007) Species concepts and species delimitation. Systematic Biology 56, 879–886.CrossRefGoogle ScholarPubMed
Doebeli, M and Dieckmann, U (2003) Speciation along environmental gradients. Nature 421, 259–264.CrossRefGoogle ScholarPubMed
Edler, D, Klein, J, Antonelli, A and Silvestro, D (2021) raxmlGUI 2.0: a graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution 12, 373–377.CrossRefGoogle Scholar
Excoffier, L and Lischer, HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Fishelson, L (2001) Community structure and fish and invertebrate biodiversity in marine ecosystems: the consequences of our actions. Boletim do Museu Municipal do Funchal 6, 331–334.Google Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Galil, BS, Boero, F, Campbell, ML, Carlton, JT, Cook, E, Fraschetti, S, Gollasch, S, Hewitt, CL, Jelmert, A, Macpherson, E, Marchini, A, McKenzie, C, Minchin, D, Occhipinti-Ambrogi, A, Ojaveer, H, Olenin, S, Piraino, S and Ruiz, GM (2015) ‘Double trouble’: the expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea. Biological Invasions 17, 973–976.CrossRefGoogle Scholar
Galindo, HM, Olson, DB and Palumbi, SR (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Current Biology 16, 1622–1626.CrossRefGoogle ScholarPubMed
Garcia, FJ and Bertsch, H (2009) Diversity and distribution of the Gastropoda Opisthobranchia from the Atlantic Ocean: a global biogeographic approach. Scientia Marina 73, 153–160.Google Scholar
Grimes, CJ, Paiva, PC, Petersen, LH and Schulze, A (2020) Rapid plastic responses to chronic hypoxia in the bearded fireworm, Hermodice carunculata (Annelida: Amphinomidae). Marine Biology 167, 140.CrossRefGoogle Scholar
Hebert, PDN, Ratnasingham, S and de Waard, JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B: Biological Sciences (suppl.) 270, S96–S99.CrossRefGoogle ScholarPubMed
Hickerson, MJ, Meyer, CP and Moritz, C (2006) DNA Barcoding will often fail to discover new animal species over broad parameter space. Systematic Biology 55, 729–739.CrossRefGoogle ScholarPubMed
Hudson, RR and Turelli, M (2003) Stochasticity overrules the “three-times rule”: genetic drift, genetic draft, and coalescence times for nuclear loci versus mitochondrial DNA. Evolution 57, 182–190.Google ScholarPubMed
Hughes, T (1994) Catastrophes, phase shifts and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551.CrossRefGoogle ScholarPubMed
Kimura, M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Kozlov, AM, Darriba, D, Flouri, T, Morel, B and Stamatakis, A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35, 4453–4455.CrossRefGoogle ScholarPubMed
Labastida-Estrada, E, Machkour-M'Rabet, S, Carrillo, L, Hénaut, Y and Castelblanco-Martίnez, DN (2019) Genetic structure of Mexican lionfish populations in the southwest Gulf of Mexico and the Caribbean Sea. PLoS ONE 14, e0222997.CrossRefGoogle ScholarPubMed
Ladd, MC and Shantz, AA (2016) Novel enemies – previously unknown predators of the bearded fireworm. Frontiers in Ecology and the Environment 14, 342–343.CrossRefGoogle Scholar
Leigh, JW and Bryant, D (2015) PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.CrossRefGoogle Scholar
Lemoine, F, Domelevo Entfellner, JB, Wilkinson, E, Correia, D, Dávila Felipe, M, De Oliveira, T and Gascuel, O (2018) Renewing Felsenstein's phylogenetic bootstrap in the era of big data. Nature 556, 452–456.CrossRefGoogle ScholarPubMed
Letunic, I and Bork, P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49, W293–W296. doi: 10.1093/nar/gkab301.CrossRefGoogle ScholarPubMed
Lucey, NM, Collins, M and Collin, R (2020) Oxygen-mediated plasticity confers hypoxia tolerance in a corallivorous polychaete. Ecology and Evolution 10, 1145–1157.CrossRefGoogle Scholar
Marsden, JR (1960) Polychaetous annelids from the shallow water around Barbados and other islands of the West Indies, with notes on larval forms. Canadian Journal of Zoology 38, 989–1020.CrossRefGoogle Scholar
Mayr, E (1942) Systematics and the Origin of Species. New York, NY: Columbia University Press.Google Scholar
Merritt, TJS, Shi, L, Chase, MC, Rex, MA, Etter, RJ and Quattro, JM (1998) Universal cytochrome b primers facilitate intraspecific studies in molluscan taxa. Molecular Marine Biology and Biotechnology 7, 7–11.Google ScholarPubMed
Miller, MW, Lohr, KE, Cameron, CM, Williams, DE and Peters, EC (2014) Disease dynamics and potential mitigation among restored and wild staghorn coral Acropora cervicornis. PeerJ 2, e541.CrossRefGoogle ScholarPubMed
Millot, C and Taupier-Letage, I (2005) Circulation in the Mediterranean Sea. In Saliot, A (ed.), The Mediterranean Sea. Handbook of Environmental Chemistry, vol. 5K. Berlin: Springer, pp. 29–66.CrossRefGoogle Scholar
Pardo, EV and Amaral, ACZ (2006) Foraging and mobility in three species of Aciculata (Annelida: Polychaeta). Brazilian Journal of Biology 66, 1065–1072.CrossRefGoogle ScholarPubMed
Patarnello, T, Volckaert, FA and Castilho, R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology 16, 4426–4444.CrossRefGoogle ScholarPubMed
Pérez, CD and Gomes, PB (2012) First record of the fireworm Hermodice carunculata (Annelida, Polychaeta) preying on colonies of the fire coral Millepora alcicornis (Cnidaria, Hydrozoa). Biota Neotropica 12, 217–219.CrossRefGoogle Scholar
Prada, C and Hellberg, ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proceedings of the National Academy of Sciences USA 110, 3961–3966.CrossRefGoogle Scholar
Prada, C, Schizas, NV and Yoshioka, PM (2008) Phenotypic plasticity or speciation? A case from a clonal marine organism. BMC Evolutionary Biology 8, 47.CrossRefGoogle ScholarPubMed
Righi, S, Maletti, I, Maltagliati, F, Castelli, A, Barbieri, M, Fai, S, Prevedelli, D and Simonini, R (2019) Morphometric and molecular characterization of an expanding Ionian population of the fireworm Hermodice carunculata (Annelida). Journal of the Marine Biological Association of the United Kingdom 99, 1569–1577.CrossRefGoogle Scholar
Righi, S, Prevedelli, D and Simonini, R (2020) Ecology, distribution and expansion of a Mediterranean native invader, the fireworm Hermodice carunculata (Annelida). Mediterranean Marine Science 21, 558–574.Google Scholar
Rίos, C, Sanz, S, Saavedra, C and Peña, JB (2002) Allozyme variation in populations of scallops, Pecten jacobaeus (L.) and P. maximus (L.) (Bivalvia: Pectinidae), across the Almeria-Oran front. Journal of Experimental Marine Biology and Ecology 267, 223–244.CrossRefGoogle Scholar
Rubinoff, D, Cameron, S and Kipling, W (2006) A genomic perspective on the shortcomings of mitochondrial DNA for “Barcoding” identification. Journal of Heredity 97, 581–594.CrossRefGoogle ScholarPubMed
Scheltema, RS (1989) Planktonic and non-planktonic development among prosobranch gastropods and its relationship to the geographic range of species. In Ryland, JS and Tyler, PA (eds), Reproduction, Genetics and Distribution of Marine Organisms. Fredensborg: Olsen and Olsen, pp. 183–188.Google Scholar
Schulze, A, Grimes, CJ and Rudek, TE (2017) Tough, armed and omnivorous: Hermodice carunculata (Annelida: Amphinomidae) is prepared for ecological challenges. Journal of the Marine Biological Association of the United Kingdom 97, 1075–1080.CrossRefGoogle Scholar
Sharp, EL, Hunter, SA and Trierweiler, RW (2005) Effects of prey and predators on the distribution and abundance of Hermodice carunculata. Hermodice Carunculata 2005, 181–184.Google Scholar
Stamatakis, A (2014) Raxml version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.CrossRefGoogle ScholarPubMed
Sussman, M, Loya, L, Fine, M and Rosenberg, E (2003) The marine fireworm Hermodice carunculata is a winter reservoir and spring summer vector for the coral bleaching pathogen Vibrio shiloi. Environmental Microbiology 5, 250–255.CrossRefGoogle Scholar
Tamura, K, Stecher, G and Kumar, S (2021) MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution. https://doi.org/10.1093/molbev/msab120.CrossRefGoogle Scholar
Thiel, M and Gutow, L (2005) The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanography and Marine Biology 43, 279–418.Google Scholar
Toso, A, Boulamail, S, Lago, N, Pierri, C, Piraino, S and Giagrande, A (2020) First description of early developmental stages of the native invasive fireworm Hermodice carunculata (Annelida, Amphinomidae): a cue to the warming of the Mediterranean Sea. Mediterranean Marine Science 21, 442–447.Google Scholar
Truelove, NK, Kough, AS, Behringer, DC, Paris, CB, Box, SJ, Preziosi, RF and Butler, MJ IV (2017) Biophysical connectivity explains population genetic structure in a highly dispersive marine species. Coral Reefs 36, 233–244.CrossRefGoogle Scholar
Vink, DLN (1974) A strange food preference of Conus aurantius. Hawaiian Shell News 12, 8.Google Scholar
Vink, DLN and von Cosel, R (1985) The Conus cedonulli complex: historical review, taxonomy and biological observations. Revue Suisse de Zoologie 92, 525–603.CrossRefGoogle Scholar
Weir, BS and Cockerham, CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
Witman, JD (1988) Effect of predation by the fireworm Hermodice carunculata on milleporid hydrocorals. Bulletin of Marine Science 42, 446–458.Google Scholar
Wolf, AT (2012) The Role of Macroalgae and the Corallivorous Fireworm Hermodice carunculata on Coral Reef Resilience in the Caribbean. PhD dissertation, Leibniz Center for Tropical Marine Ecology (ZMT).CrossRefGoogle Scholar
Wolf, AT and Nugues, MM (2013) Predation on coral settlers by the corallivorous fireworm Hermodice carunculata. Coral Reefs 32, 227–231.CrossRefGoogle Scholar
Wolf, AT, Nugues, MM and Wild, C (2014) Distribution, food preference, and trophic position of the corallivorous fireworm Hermodice carunculata in a Caribbean coral reef. Coral Reefs 33, 1153–1163.CrossRefGoogle Scholar
Yáñez-Rivera, B and Salazar-Vallejo, SI (2011) Revision of Hermodice Kinberg, 1857 (Polychaeta: Amphinomidae). Scientia Marina 75, 251–262.CrossRefGoogle Scholar
Zardoya, R, Castilho, R, Grande, C, Favre-Krey, L, Caetano, S, Marcato, S, Krey, G and Patarnello, T (2004) Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus) in the Mediterranean Sea. Molecular Ecology 13, 1785–1798.CrossRefGoogle Scholar
Zardus, JD and Hadfield, MG (2005) Multiple origins and incursions of the Atlantic barnacle Chthamalus proteus in the Pacific. Molecular Ecology 14, 3719–3733.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Cruz Ramos and Schizas supplementary material

Cruz Ramos and Schizas supplementary material 1

Download Cruz Ramos and Schizas supplementary material(PDF)
PDF 169.4 KB
Supplementary material: PDF

Cruz Ramos and Schizas supplementary material

Cruz Ramos and Schizas supplementary material 2

Download Cruz Ramos and Schizas supplementary material(PDF)
PDF 362.6 KB