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The sibling polychaetes Platynereis dumerilii and Platynereis massiliensis in the Mediterranean Sea: are phylogeographic patterns related to exposure to ocean acidification?

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Abstract

High pCO2 environments, such as volcanic carbon dioxide (CO2) vents, which mimic predicted near-future scenarios of ocean acidification (OA), offer an opportunity to examine effects of low pH conditions on marine biodiversity and adaptation/acclimatization of marine organisms to such conditions. Based on previous field studies in these systems, it is predicted that the stress owing to increasing CO2 concentrations favours the colonization by invertebrate species with a brooding habit. The goal of this study was to investigate the relative occurrence of the two sibling species Platynereis dumerilii (Audouin & Milne-Edwards, 1834) (free spawner) and Platynereis massiliensis (Moquin-Tandon, 1869) (egg brooder) in two shallow CO2 vents off Ischia and Vulcano islands (Italy, Tyrrhenian Sea), and in various areas with ambient pH conditions, where they represent one of the dominant genera. Phylogeographic analyses were integrated with reproductive biology and life-history observations on some selected populations thriving in the vent areas. This approach revealed the presence of four distinct Platynereis clades. Whereas two clades primarily inhabit CO2 vents and are presumably all brooders, the other two clades dominate the non-acidified sites and appear to be epitokous free spawners. We postulate that one of the brooding, vent-inhabiting clades represents P. massiliensis and one of the free spawning, non-vent-inhabiting clades represents P. dumerilii, although confirmation of the species status with sequence data from the respective-type localities would be desirable.

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References

  • Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  Google Scholar 

  • Bellan G (1980) Relationship of pollution to rocky substratum polychaetes on the French Mediterranean coast. Mar Pollut Bull 1:318–321

    Article  Google Scholar 

  • Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155

    Article  Google Scholar 

  • Blake JA, Grassle JP, Eckelbarger KJ (2009) Capitella teleta a new species designation for the opportunistic and experimental Capitella sp I with a review of the literature for confirmed records. Zoosymposia 2:25–53

    Google Scholar 

  • Boatta F, D’Alessandro W, Gagliano AL, Liotta M, Milazzo M, Rodolfo-Metalpa R, Hall-Spencer JM, Parello F (2013) Geochemical survey of Levante Bay Vulcano Island (Italy) a natural laboratory for the study of ocean acidification. Mar Pollut Bull 73(2):485–494

    Article  CAS  Google Scholar 

  • Boore JL, Brown WM (2000) Mitochondrial genomes of Galathealinum, Helobdella and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol Biol Evol 17(1):87–106

    Article  CAS  Google Scholar 

  • Burlinson FC, Lawrence AJ (2007) A comparison of acute and chronic toxicity tests used to examine the temporal stability of a gradient in copper tolerance of Hediste diversicolor from the Fal estuary, Cornwall, UK. Mar Pollut Bull 54:66–71

    Article  CAS  Google Scholar 

  • Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    Article  CAS  Google Scholar 

  • Calosi P, Rastrick SPS, Lombardi C, de Guzman HJ, Davidson L, Jahnke M, Giangrande A, Hardege JD, Schulze A, Spicer JI, Gambi MC (2013) Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system. Phil Trans R Soc Lond B Biol Sci 368:20120444. doi:10.1098/rstb20120444

    Article  Google Scholar 

  • Castelli A, Bianchi CN, Cantone G, Çinar ME, Gambi MC, Giangrande A, IraciSareri D, Lanera P, Licciano M, Musco L, Sanfilippo R, Simonini R (2008) Annelida Polychaeta. In: Relini G (ed) Checklist della flora e della fauna dei mari italiani. Parte I Biol Mar Mediterr 15(1):323–373

  • Dean HK (2008) The use of polychaetes (Annelida) as indicator species of marine pollution: a review. Rev Biol Trop 56:11–38

    Google Scholar 

  • Durou C, Smith BD, Roméo M, Rainbow PS, Mouneyrac C, Mouloud M, Gnassia-Barelli M, Gillet P, Deutsch B, Amiard-Triquet C (2007) From biomarkers to population responses in Nereis diversicolor: assessment of stress in estuarine ecosystems. Ecotoxicol Environ Saf 66:402–411

    Article  CAS  Google Scholar 

  • Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1:165–169

    Article  CAS  Google Scholar 

  • Fischer A, Dorresteijn A (2004) The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage lifelong segment proliferation and a mixed benthic/pelagic life cycle. BioEssays 26:314–325

    Article  Google Scholar 

  • Fischlin A, Midgley GF, Price J, Leemans R, Gopal B, Turley C, Rounsevell M, Dube P, Tarazona J, Velichko A (2007) Ecosystems their properties goods and services. In: Parry ML (ed) Climate Change 2007: Impacts Adaptation and Vulnerability Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change Ecosystems their properties goods and services. Cambridge University Press, Cambridge, pp 211–272

    Google Scholar 

  • Folmer O, Black M, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  Google Scholar 

  • Gambi MC, Zupo V, Buia MC, Mazzella L (2000) Feeding ecology of Platynereis dumerilii (Audouin & Milne-Edwards) in the seagrass Posidonia oceanica system: the role of the epiphytic flora (Polychaeta, Nereididae). Ophelia 53(3):189–202

    Article  Google Scholar 

  • Gambi MC, Musco L, Giangrande A, Badalamenti F, Micheli F, Kroeker KJ (2016) Distribution and functional traits of polychaetes in a CO2 vent system: winners and losers among closely related species. Mar Ecol Prog Ser 550:121–134

    Article  CAS  Google Scholar 

  • Gattuso JP, Hansson L (eds) (2011) Ocean acidification. Oxford University Press, New York

    Google Scholar 

  • Gattuso JP, Lavigne H (2009) Technical note: approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6:2121–2133

    Article  CAS  Google Scholar 

  • Giangrande A, Fraschetti S, Terlizzi A (2002) Local recruitment differences in Platynereis dumerilii (Polychaeta Nereididae) and their consequences for population structure. Ital J Zool 69:133–139

    Article  Google Scholar 

  • Glasby CJ, Hsieh HL (2006) New species and new records of the Perinereis nuntia species group (Nereididae: Polychaeta) from Taiwan and other Indo-West Pacific shores. Zool Stud 45:553–577

    Google Scholar 

  • Grassle JP, Grassle JF (1976) Sibling species in the marine pollution indicator Capitella (Polychaeta). Science 192:567–569

    Article  CAS  Google Scholar 

  • Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99. doi:10.1038/nature07051

    Article  CAS  Google Scholar 

  • Hardege JD, Bartels-Hardege HD, Zeeck E, Grimm FT (1990) Induction of swarming in Nereis succinea. Mar Biol 104:291–294

    Article  Google Scholar 

  • Harvey BP, Al-Janabi B, Broszeit S, Cioffi R, Kumar A, Aranguren-Gassis M, Bailey A, Green L, Gsottbauer CM, Hall EF, Lechler ML, Mancuso FP, Pereira CO, Ricevuto E, Schram JB, Stapp LS, Stenberg S, Santa Rosa LT (2014) Evolution of marine organisms under climate change at different levels of biological organisation. Water 6:3545–3574

    Article  Google Scholar 

  • Hauenschild C (1951) Nachweis de sogenannten atoken Geschlechtsform des Polychaeten Platynereis dumerilii Aud et M Edw als eigene Art auf Grund von Zuchtversuchen. Zoolo Jahr Abteil all Zool Physiol der Tiere 63:107–128

    Google Scholar 

  • Helm C, Adamo H, Hourdez S, Bleidorn C (2014) An immunocytochemical window into the development of Platynereis massiliensis (Annelida Nereididae). Int J Dev Biol 58:613–622

    Article  Google Scholar 

  • IPCC Climate Change (2013) The Physical Science Basis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernamental Panel on Climate Change. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Cambridge University Press, Cambridge, pp 1–33

  • Johnson VR, Brownlee C, Rickaby REM, Graziano M, Milazzo M, Hall-Spencer JM (2013) Responses of marine benthic microalgae to elevated CO2. Mar Biol 160:1813–1824

    Article  CAS  Google Scholar 

  • Kroeker KJ, Micheli F, Gambi MC, Martz TR (2011) Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc Natl Acad Sci USA 108:14515–14520

    Article  CAS  Google Scholar 

  • Kumar A, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  Google Scholar 

  • Lewis C, Karageorgopoulos P (2008) A new species of Marphysa (Eunicidae) from the western Cape of South Africa. J Mar Biol Assoc UK 88:277–287

    Article  Google Scholar 

  • Lucey NM, Lombardi C, De Marchi L, Schulze A, Gambi MC, Calosi P (2015) To brood or not to brood: are marine invertebrates that protect their offspring more resilient to ocean acidification? Nat Sci Rep 5:12009. doi:10.1038/srep12009

    Article  Google Scholar 

  • Lucey NL, Lombardi C, Florio M, De Marchi L, Nannini M, Rundle S, Gambi MC, Calosi P (2016) No evidence of local adaptation to low pH in a calcifying polychaete population from a shallow CO2 vent system. Evolut Appl. doi:10.1111/eva.12400

    Google Scholar 

  • Mikac B (2015) A sea of worms: polychaete checklist of the Adriatic Sea. Zootaxa 3943(1):1–172

    Article  Google Scholar 

  • Miller JR, Koren S, Sutton G (2010) Assembly algorithms for next-generation sequencing data. Genomics 95(6):315–327

    Article  CAS  Google Scholar 

  • Moquin-Tandon A (1869) Note sur une nouvelle Annèlide hermaphrodite. Ann Sc Nat 11:34

    Google Scholar 

  • Nygren A (2014) Cryptic polychaete diversity: a review. Zoolog Scr 43:172–183

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic divergence reproductive isolation and marine speciation. Ann Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Raible F, Tessmar-Raible K, Osoegawa K, Wincker P, Jubin C, Balavoine G, Ferrier D, Benes V, de Jong P, Weissenbach J, Bork P, Arendt D (2005) Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science 310:1325–1326

    Article  CAS  Google Scholar 

  • Reish DJ, Anderson FE, Horn KM, Hardege JD (2014) Molecular phylogenetics of the Neanthes acuminata (Annelida: Nereididae) species complex. Mem Mus Vic 71:271–278

    Article  Google Scholar 

  • Ricevuto E, Kroeker KJ, Ferrigno F, Micheli F, Gambi MC (2014) Spatio-temporal variability of polychaete colonization at volcanic CO2 vents indicates high tolerance to ocean acidification. Mar Biol 161:2909–2919

    Article  CAS  Google Scholar 

  • Ricevuto E, Benedetti M, Regoli F, Spicer JI, Gambi MC (2015a) Antioxidant capacity of polychaetes occurring along a natural pCO2 gradient: results of an in situ reciprocal transplant experiment. Mar Environ Res 112(Part A):44–51

    Article  CAS  Google Scholar 

  • Ricevuto E, Vizzini S, Gambi MC (2015b) Ocean acidification effects on stable isotope signatures and trophic interactions of polychaete consumers and organic matter sources at a CO2 shallow vent system. J Exp Mar Biol Ecol 468:105–117

    Article  Google Scholar 

  • Ricevuto E, Lanzoni I, Fattorini D, Regoli F, Gambi MC (2016) Arsenic speciation and susceptibility to oxidative stress in the fanworm Sabella spallanzanii (Gmelin) (Annelida Sabellidae) under naturally acidified conditions: an in situ transplant experiment in a Mediterranean CO2 vent system. Sci Total Environ 544:765–773

    Article  CAS  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 32: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542

    Article  Google Scholar 

  • Saderne V, Wahl M (2012) Effect of Ocean acidification on growth, calcification and recruitment of calcifying and non-calcifying epibionts of brown algae. Biogeosci Discuss 9:3739–3766

    Article  Google Scholar 

  • Sato M, Masuda Y (1997) Genetic differentiation in two sibling species of the brackish-water polychaete Hediste japonica complex (Nereididae). Mar Biol 130:163–170

    Article  CAS  Google Scholar 

  • Sato M, Nakashima A (2003) A review of Asian Hediste species complex (Nereididae Polychaeta) with descriptions of two new species and a redescription of Hediste japonica (Izuka 1908). Zool J Linn Soc 137:403–445

    Article  Google Scholar 

  • Sato M, Tsuchiya M (1991) Two patterns of early development in nereidid polychaetes keying out to Neanthes japonica (Izuka). Ophelia 5(Suppl):371–382

    Google Scholar 

  • Schneider S, Fischer A, Dorresteijn AW (1992) A morphometric comparison of dissimilar early development in sibling species of Platynereis (Annelida Polychaeta). Roux’s Arch Dev Biol 201:243–256

    Article  Google Scholar 

  • Teske PR, Papadopoulos I, Zardi GI, McQuaid CD, Edkins MT, Griffiths CL, Barker NP (2007) Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development. Mar Biol 152:697–711

    Article  Google Scholar 

  • Turner LM, Ricevuto E, Massa-Gallucci A, Gambi MC, Calosi P (2015) Energy metabolism and cellular homeostasis trade-offs provide the basis for a new type of sensitivity to ocean acidification in a marine polychaete at a high CO2 vent: adenylate and phosphagen energy pools versus carbonic anhydrase. J Exp Biol 163:211. doi:10.1242/jeb117705

    Google Scholar 

  • Valvassori G, Massa-Gallucci A, Gambi MC (2015) Reappraisal of Platynereis massiliensis (Moquin-Tandon) (Annelida Nereididae) a neglected sibling species of Platynereis dumerilii (Audouin & Milne Edwards). Biol Mar Mediterr 22(1):113–116

    Google Scholar 

  • Vázquez-Núñez R, Méndez N, Green-Ruíz C (2007) Bioaccumulation and elimination of Hg in the fireworm Eurythoe complanata (Annelida: Polychaeta) from Mazatlan, Mexico. Arch Environ Contam Toxicol 52(4):541

    Article  Google Scholar 

  • Vieitez J, Alos C, Parapar J et al (2004) Fauna Iberica, Vol 25. Annelida Polychaeta I. Consejo Superior de Investigaciones Cientificas, Madrid, p 536

  • Virgilio M, Maci S, Abbiati M (2005) Comparisons of genotype-tolerance responses in populations of Hediste diversicolor (Polychaeta: Nereididae) exposed to copper stress. Mar Biol 147:1305–1312

    Article  CAS  Google Scholar 

  • Virgilio M, Fauvelot C, Costantini F, Abbiati M, Backeljau T (2009) Phylogeography of the common ragworm Hediste diversicolor (Polychaeta: Nereididae) reveals cryptic diversity and multiple colonization events across its distribution. Mol Ecol 18(9):1980–1994

    Article  CAS  Google Scholar 

  • Vizzini S, Martínez-Crego B, Andolina C, Massa-Gallucci A, Connell SD, Gambi MC (2017) Ocean acidification as a driver of community simplification via the collapse of higher-order and rise of lower-order consumers. Nat Sci Rep 7:4018. doi:10.1038/s41598-017-03802-w

    Article  CAS  Google Scholar 

  • Zantke J, Bannister S, Rajan VBV, Raible F, Tessmar-Raible K (2014) Genetic and genomic tools for the marine annelid Platynereis dumerilii. Genet Soc Am 197(1):19–31. doi:10.1534/genetics.112.148254

    CAS  Google Scholar 

  • Zeeck E, Hardege JD, Bartels-Hardege H, Wesselmann G (1988) Sex pheromone in a marine polychaete: determination of the chemical structure. J Exp Zool part A 246(3):285–292

    Article  CAS  Google Scholar 

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Acknowledgements

This project was supported by an EU-ASSEMBLE Grant to JDH, JW, and MCG and partially by National Science Foundation Grant DEB-1036186 to AS. GV was supported by a Stazione Zoologica Anton Dohrn PhD fellowship. We thank A. Massa-Gallucci for some early observation on P. massiliensis brooding in the laboratory on the Ischia vent’s population, and Thomas Larsson for collaboration in the collection of heteronerids at the Castello vents. MCG is indebted to Prof. Vizzini S. (University of Palermo) and the ESF COST Action (ES 0906) “Seagrass Productivity: From Genes to Ecosystem Management” for the invitation at the Workshop in Vulcano island in early May 2013, and the opportunity to sample Platynereis specimens at the vents.

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Correspondence to Giulia Valvassori.

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This project was supported by an EU-ASSEMBLE Grant to JDH, JW and MCG and partially by National Science Foundation Grant DEB-1036186 to AS. GV was supported by a Stazione Zoologica Anton Dohrn PhD fellowship.

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Wäge, J., Valvassori, G., Hardege, J.D. et al. The sibling polychaetes Platynereis dumerilii and Platynereis massiliensis in the Mediterranean Sea: are phylogeographic patterns related to exposure to ocean acidification?. Mar Biol 164, 199 (2017). https://doi.org/10.1007/s00227-017-3222-x

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