Skip to main content
SpringerLink
Log in

Phylogeography of two intertidal seaweeds, Gelidium lingulatum and G. rex (Rhodophyta: Gelidiales), along the South East Pacific: patterns explained by rafting dispersal?

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Rafting on floating seaweeds facilitates dispersal of associated organisms, but there is little information on how rafting affects the genetic structure of epiphytic seaweeds. Previous studies indicate a high presence of seaweeds from the genus Gelidium attached to floating bull kelp Durvillaea antarctica (Chamisso) Hariot. Herein, we analyzed the phylogeographic patterns of Gelidium lingulatum (Kützing 1868) and G. rex (Santelices and Abbott 1985), species that are partially co-distributed along the Chilean coast (28°S–42°S). A total of 319 individuals from G. lingulatum and 179 from G. rex (20 and 11 benthic localities, respectively) were characterized using a mitochondrial marker (COI) and, for a subset, using a chloroplastic marker (rbcL). Gelidium lingulatum had higher genetic diversity, but its genetic structure did not follow a clear geographic pattern, while G. rex had less genetic diversity with a shallow genetic structure and a phylogeographic break coinciding with the phylogeographic discontinuity described for this region (29°S–33°S). In G. lingulatum, no isolation-by-distance was observed, in contrast to G. rex. The phylogeographic pattern of G. lingulatum could be explained mainly by rafting dispersal as an epiphyte of D. antarctica, although other mechanisms cannot be completely ruled out (e.g., human-mediated dispersal). The contrasting pattern observed in G. rex could be attributed to other factors such as intertidal distribution (i.e., G. rex occurs in the lower zone compared to G. lingulatum) or differential efficiency of recruitment after long-distance dispersal. This study indicates that rafting dispersal, in conjunction with the intertidal distribution, can modulate the phylogeographic patterns of seaweeds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alberto F, Santos R, Leitão JM (1999) Assessing patterns of geographic dispersal of Gelidium sesquipedale (Rhodophyta) through RAPD differentiation of populations. Mar Ecol Prog Ser 191:101–108. doi:10.3354/Meps191101

    Article  Google Scholar 

  • Alberto F, Raimondi PT, Reed DC, Coelho NC, Leblois R, Whitmer A, Serrão EA (2010) Habitat continuity and geographic distance predict population genetic differentiation in giant kelp. Ecology 91:49–56. doi:10.1890/09-0050.1

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2

    Article  CAS  Google Scholar 

  • Aravena G, Broitman B, Stenseth NC (2014) Twelve years of change in coastal upwelling along the central-northern coast of Chile: spatially heterogeneous responses to climatic variability. PLoS One 9:e90276. doi:10.1371/journal.pone.0090276

    Article  CAS  Google Scholar 

  • Astudillo JC, Bravo M, Dumont CP, Thiel M (2009) Detached aquaculture buoys in the SE Pacific: potential dispersal vehicles for associated organisms. Aquat Biol 5:219–231. doi:10.3354/ab00151

    Article  Google Scholar 

  • Ballard JW, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744. doi:10.1046/j.1365-294X.2003.02063.x

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Banks NC, Paini DR, Bayliss KL, Hodda M (2015) The role of global trade and transport network topology in the human-mediated dispersal of alien species. Ecol Lett 18:188–199. doi:10.1111/ele.12397

    Article  Google Scholar 

  • Billard E, Daguin C, Pearson G, Serrão E, Engel C, Valero M (2005) Genetic isolation between three closely related taxa: Fucus vesiculosus, F. spiralis, and F. ceranoides (Phaeophyceae). J Phycol 41:900–905. doi:10.1111/j.0022-3646.2005.04221.x

    Article  Google Scholar 

  • Bobadilla M, Santelices B (2005) Variations in the dispersal curves of macroalgal propagules from a source. J Exp Mar Biol Ecol 327:47–57. doi:10.1016/j.jembe.2005.06.006

    Article  Google Scholar 

  • Boo GH, Park JK, Boo SM (2013) Gelidiophycus (Rhodophyta: Gelidiales): a new genus of marine algae from East Asia. Taxon 62:1105–1116. doi:10.12705/626.7

    Article  Google Scholar 

  • Boo GH, Mansilla A, Nelson W, Bellgrove A, Boo SM (2014a) Genetic connectivity between trans-oceanic populations of Capreolia implexa (Gelidiales, Rhodophyta) in cool temperate waters of Australasia and Chile. Aquat Bot 119:73–79. doi:10.1016/j.aquabot.2014.08.004

    Article  Google Scholar 

  • Boo GH, Kim KM, Nelson WA, Riosmena-Rodríguez R, Yoon KJ, Boo SM (2014b) Taxonomy and distribution of selected species of the agarophyte genus Gelidium (Gelidiales, Rhodophyta). J Appl Phycol 26:1243–1251. doi:10.1007/s10811-013-0111-7

    Article  Google Scholar 

  • Boo GH, Le Gall L, Miller KA, Freshwater DW, Wernberg T, Terada R, Yoon KJ, Boo SM (2016) A novel phylogeny of the Gelidiales (Rhodophyta) based on five genes including the nuclear CesA, with descriptions of Orthogonacladia gen. nov and Orthogonacladiaceae fam. nov. Mol Phylogenet Evol 101:359–372. doi:10.1016/j.ympev.2016.05.018

    Article  CAS  Google Scholar 

  • Bouza N, Caujape-Castells J, González-Pérez MA, Sosa PA (2006) Genetic structure of natural populations in the red algae Gelidium canariense (Gelidiales, Rhodophyta) investigated by random amplified polymorphic DNA (RAPD) markers. J Phycol 42:304–311. doi:10.1111/j.1529-8817.2006.00201.x

    Article  CAS  Google Scholar 

  • Broitman BR, Navarrete SA, Smith F, Gaines SD (2001) Geographic variation of southeastern Pacific intertidal communities. Mar Ecol Prog Ser 224:21–34. doi:10.3354/Meps224021

    Article  Google Scholar 

  • Camus PA (2001) Biogeografía marina de Chile continental. Rev Chil Hist Nat 74:587–617

    Article  Google Scholar 

  • Castilla JC, Manríquez PH, Camaño A (2010) Effects of rocky shore coseismic uplift and the 2010 Chilean mega-earthquake on intertidal biomarker species. Mar Ecol Prog Ser 418:17–23. doi:10.3354/meps08830

    Article  Google Scholar 

  • Coyer JA, Hoarau G, Costa JF, Hogerdijk B, Serrão EA, Billard E, Valero M, Pearson GA, Olsen JL (2011a) Evolution and diversification within the intertidal brown macroalgae Fucus spiralis/F. vesiculosus species complex in the North Atlantic. Mol Phylogenet Evol 58:283–296. doi:10.1016/j.ympev.2010.11.015

    Article  CAS  Google Scholar 

  • Coyer JA, Hoarau G, Van Schaik J, Luijckx P, Olsen JL (2011b) Trans-Pacific and trans-Arctic pathways of the intertidal macroalga Fucus distichus L. reveal multiple glacial refugia and colonizations from the North Pacific to the North Atlantic. J Biogeogr 38:756–771. doi:10.1111/j.1365-2699.2010.02437.x

    Article  Google Scholar 

  • Cumming RA, Nikula R, Spencer HG, Waters JM (2014) Transoceanic genetic similarities of kelp-associated sea slug populations: long-distance dispersal via rafting? J Biogeogr 41:2357–2370. doi:10.1111/jbi.12376

    Article  Google Scholar 

  • Dawson MN, Hays CG, Grosberg RK, Raimondi PT (2014) Dispersal potential and population genetic structure in the marine intertidal of the eastern North Pacific. Ecol Monogr 84:435–456. doi:10.1890/13-0871.1

    Article  Google Scholar 

  • Destombe C, Godin J, Lefebvre C, Dehorter O, Vernet P (1992) Differences in dispersal abilities of haploid and diploid spores of Gracilaria verrucosa (Gracilariales, Rhodophyta). Bot Mar 35:93–98. doi:10.1515/botm.1992.35.2.93

    Article  Google Scholar 

  • Dixon PS, Irvine LM (1977) Seaweeds of the British Isles. Volume 1. Rhodophyta. Part 1. Introduction, Nemaliales, Gigartinales. The Natural History Museum, London, p 252

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581. doi:10.1046/j.1365-294X.2002.01650.x

    Article  CAS  Google Scholar 

  • Engel CR, Destombe C, Valero M (2004) Mating system and gene flow in the red seaweed Gracilaria gracilis: effect of haploid-diploid life history and intertidal rocky shore landscape on fine-scale genetic structure. Heredity 92:289–298. doi:10.1038/sj.hdy.6800407

    Article  CAS  Google Scholar 

  • Engel CR, Billard E, Voisin M, Viard F (2008) Conservation and polymorphism of mitochondrial intergenic sequences in brown algae (Phaeophyceae). Eur J Phycol 43:195–205. doi:10.1080/09670260701823437

    Article  CAS  Google Scholar 

  • Ewers-Saucedo C, Pringle JM, Sepúlveda HH, Byers JE, Navarrete SA, Wares JP (2016) The oceanic concordance of phylogeography and biogeography: a case study in Notochthamalus. Ecol Evol 6:4403–4420. doi:10.1002/ece3.2205

    Article  Google Scholar 

  • Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864. doi:10.1046/j.1365-294X.2003.02004.x

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin (version 3.5): arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  Google Scholar 

  • Försterra G (2009) Ecological and biogeographical aspects of the Chilean Fjord region. In: Häussermann V, Försterra G (eds) Marine benthic fauna of chilean patagonia. Nature in Focus, Puerto Montt, pp 61–76

    Google Scholar 

  • Fraser CI, Nikula R, Spencer HG, Waters JM (2009a) Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum. Proc Natl Acad Sci USA 106:3249–3253. doi:10.1073/pnas.0810635106

    Article  CAS  Google Scholar 

  • Fraser CI, Hay CH, Spencer HG, Waters JM (2009b) Genetic and morphological analyses of the southern bull kelp Durvillaea antarctica (Phaeophyceae: Durvillaeales) in New Zealand reveal cryptic species. J Phycol 45:436–443. doi:10.1111/j.1529-8817.2009.00658.x

    Article  CAS  Google Scholar 

  • Fraser CI, Thiel M, Spencer HG, Waters JM (2010) Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp. BMC Evol Biol 10:203. doi:10.1186/1471-2148-10-203

    Article  CAS  Google Scholar 

  • Freshwater DW, Rueness J (1994) Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33:187–194. doi:10.2216/i0031-8884-33-3-187.1

    Article  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  Google Scholar 

  • Gavio B, Fredericq S (2002) Grateloupia turuturu (Halymeniaceae, Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora. Eur J Phycol 37:349–359. doi:10.1017/s0967026202003839

    Article  Google Scholar 

  • Gómez IM, Westermeier RC (1991) Frond regrowth from basal disc in Iridaea laminarioides (Rhodophyta, Gigartinales) at Mehuín, southern Chile. Mar Ecol Prog Ser 73:83–91. doi:10.3354/meps073083

    Article  Google Scholar 

  • González S, Stotz W, Toledo P, Jorquera M, Romero M (1991) Utilización de diferentes microambientes del intermareal como lugares de asentamiento por Fissurella spp (Gastropoda: Prosobranchia) (Palo Colorado, Los Vilos, Chile). Rev Biol Mar Oceanogr 26: 325–338. http://www.revbiolmar.cl/escaneados/262-325.pdf. Accessed 29 Aug 2016

  • González A, Beltrán J, Hiriart-Bertrand L, Flores V, de Reviers B, Correa JA, Santelices B (2012) Identification of cryptic species in the Lessonia nigrescens complex (Phaeophyceae, Laminariales). J Phycol 48:1153–1165. doi:10.1111/j.1529-8817.2012.01200.x

    Article  Google Scholar 

  • Grant SW (2016) Paradigm shifts in the phylogeographic analysis of seaweeds. In: Hu ZM, Fraser CI (eds) Seaweed phylogeography. Springer, Dordrecht, pp 23–62. doi:10.1007/978-94-017-7534-2_2

  • Guillemin ML, Valero M, Faugeron S, Nelson W, Destombe C (2014) Tracing the trans-pacific evolutionary history of a domesticated seaweed (Gracilaria chilensis) with archaeological and genetic data. PLoS One 9:e114039. doi:10.1371/journal.pone.0114039

    Article  CAS  Google Scholar 

  • Guillemin ML, Valero M, Tellier F, Macaya EC, Destombe C, Faugeron S (2016a) Phylogeography of seaweeds in the South East Pacific: complex evolutionary processes along a latitudinal gradient In: Hu ZM, Fraser CI (eds) Seaweed Phylogeography. Springer, Dordrecht, pp 251–278. doi:10.1007/978-94-017-7534-2_10

  • Guillemin ML, Contreras-Porcia L, Ramírez ME, Macaya EC, Bulboa-Contador C, Woods H, Wyatt C, Brodie J (2016b) The bladed Bangiales (Rhodophyta) of the South Eastern Pacific: molecular species delimitation reveals extensive diversity. Mol Phylogenet Evol 94:814–826. doi:10.1016/j.ympev.2015.09.027

    Article  Google Scholar 

  • Guo B, Wares JP (2017) Large-scale gene flow in the barnacle Jehlius cirratus and contrasts with other broadly-distributed taxa along the Chilean coast. PeerJ 5:e2971. doi:10.7717/peerj.2971

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Haye PA, Varela AI, Thiel M (2012) Genetic signatures of rafting dispersal in algal-dwelling brooders Limnoria spp. (Isopoda) along the SE Pacific (Chile). Mar Ecol Prog Ser 455:111–122. doi:10.3354/meps09673

    Article  Google Scholar 

  • Haye PA, Segovia NI, Muñoz-Herrera NC, Gálvez FE, Martínez A, Meynard A, Pardo-Gandarillas MC, Poulin E, Faugeron S (2014) Phylogeographic structure in benthic marine invertebrates of the southeast Pacific coast of Chile with differing dispersal potential. PLoS One 9:e88613. doi:10.1371/journal.pone.0088613

    Article  CAS  Google Scholar 

  • Hernández CJ (1997) Análisis de la variación estacional e interanual de la cosecha de Gelidium robustum en Baja California Sur, México. Master thesis, Centro Interdisciplinario de Ciencias Marinas, La Paz, Baja California Sur, México

  • Hinojosa IA, Pizarro M, Ramos M, Thiel M (2010) Spatial and temporal distribution of floating kelp in the channels and fjords of southern Chile. Estuar Coast Shelf Sci 87:367–377. doi:10.1016/j.ecss.2009.12.010

    Article  Google Scholar 

  • Hinojosa IA, Rivadeneira MM, Thiel M (2011) Temporal and spatial distribution of floating objects in coastal waters of central-southern Chile and Patagonian fjords. Cont Shelf Res 31:172–186. doi:10.1016/j.csr.2010.04.013

    Article  Google Scholar 

  • Hoffmann A, Santelices B (1997) Flora marina de Chile Central. Ediciones Universidad Católica de Chile, Santiago de Chile

    Google Scholar 

  • Hu ZM, De-Lin D, López-Baptista J (2016) Seaweed phylogeography from 1994 to 2014: an overview. In: Hu ZM, Fraser CI (eds) Seaweed Phylogeography. Springer, Dordrecht, pp 3–22. doi:10.1007/978-94-017-7534-2_1

  • Jaramillo E, Dugan JE, Hubbard DM, Melnick D, Manzano M, Duarte C, Campos C, Sánchez R (2012) Ecological implications of extreme events: footprints of the 2010 earthquake along the Chilean coast. PLoS One 7:8. doi:10.1371/journal.pone.0035348

    Article  CAS  Google Scholar 

  • John D, Paterson G, Evans N, Ramírez M, Spencer J, Báez P, Ferrero T, Valentine C, Reid D (2003) Manual de biotopos marinos de la región de Aysén, Sur de Chile (A manual of marine biotopes of Region Aysén, Southern Chile. The Laguna San Raphael National Park, Estero Elefantes, Chonos Archipelago and Katalalixar). The Natural History Museum, London

  • Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the Northeastern Pacific rocky intertidal community. PLoS One 5:13. doi:10.1371/journal.pone.0008594

    Google Scholar 

  • Kiessling T, Gutow L, Thiel M (2015) Marine litter as habitat and dispersal vector. In: Bergmann M, Gutow L, Klages K (eds) Marine anthropogenic litter, Springer, Berlin, pp 141–184. doi:10.1007/978-3-319-16510-3_6

  • Kim KM, Boo SM (2012) Phylogenetic relationships and distribution of Gelidium crinale and G. pusillum (Gelidiales, Rhodophyta) using cox1 and rbcL sequences. Algae 27:83–94. doi:10.4490/algae.2012.27.2.083

    Article  Google Scholar 

  • Kim KM, Hwang IK, Park JK, Boo SM (2011) A new agarophyte species, Gelidium eucorneum sp. nov. (Gelidiales, Rhodophyta), based on molecular and morphological data. J Phycol 47:904–910. doi:10.1111/j.1529-8817.2011.01005.x

    Article  Google Scholar 

  • Kim KM, Hoarau GG, Boo SM (2012) Genetic structure and distribution of Gelidium elegans (Gelidiales, Rhodophyta) in Korea based on mitochondrial cox1 sequence data. Aquat Bot 98:27–33. doi:10.1016/j.aquabot.2011.12.005

    Article  Google Scholar 

  • Krueger-Hadfield SA, Hoban SM (2016) The importance of effective sampling for exploring the population dynamics of haploid–diploid seaweeds. J Phycol 52:1–9. doi:10.1111/jpy.12366

    Article  Google Scholar 

  • Krueger-Hadfield SA, Roze D, Mauger S, Valero M (2013) Intergametophytic selfing and microgeographic genetic structure shape populations of the intertidal red seaweed Chondrus crispus. Mol Ecol 22:3242–3260. doi:10.1111/mec.12191

    Article  CAS  Google Scholar 

  • Kützing FT (1868) Tabulae phycologicae; oder, Abbildungen der Tange. Vol. XVIII pp. [i–iii], 1–35, 100 pls. Nordhausen: Gedruckt auf kosten des Verfassers (in commission bei W. Köhne)

  • Lachkar Z, Gruber N (2012) A comparative study of biological production in eastern boundary upwelling systems using an artificial neural network. Biogeosciences 9:293–308. doi:10.5194/bg-9-293-2012

    Article  Google Scholar 

  • Lin SM, Fredericq S, Hommersand MH (2001) Systematics of the Delesserlaceae (Ceramiales, Rhodophyta) based on large subunit rDNA and rbcL sequences, including the Phycodryoideae, subfam. nov. J Phycol 37:881–899. doi:10.1046/j.1529-8817.2001.01012.x

    Article  CAS  Google Scholar 

  • Lindstrom SC, Gabrielson PW, Hughey JR, Macaya EC, Nelson WA (2015) Sequencing of historic and modern specimens reveals cryptic diversity in Nothogenia (Scinaiaceae, Rhodophyta). Phycologia 54:97–108. doi:10.2216/14-077.1

    Article  CAS  Google Scholar 

  • López B, Macaya EC, Tellier F, Tala F, Thiel M (2017) The variable routes of rafting: stranding dynamics of floating bull-kelp Durvillaea antarctica (Fucales, Phaeophyceae) on beaches in the SE Pacific. J Phycol 54:70–84. doi:10.1111/jpy.12479

    Article  Google Scholar 

  • Macaya EC, Zuccarello GC (2010a) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol Prog Ser 420:103–112. doi:10.3354/meps08893

    Article  Google Scholar 

  • Macaya EC, Zuccarello GC (2010b) DNA barcoding and genetic divergence in the giant kelp Macrocystis (Laminariales). J Phycol 46:736–742. doi:10.1111/j.1529-8817.2010.00845.x

    Article  CAS  Google Scholar 

  • Macaya EC, López B, Tala F, Tellier F, Thiel M (2016) Float and raft: role of buoyant seaweeds in the phylogeography and genetic structure of non-buoyant associated flora. In: Hu ZM, Fraser CI (eds) Seaweed phylogeography, Springer, Dordrecht, pp 97–130. doi:10.1007/978-94-017-7534-2_4

  • Matsuhiro B, Urzúa CC (1990) Agars from Gelidium rex (Gelidiales, Rhodophyta). Hydrobiologia 204:545–549. doi:10.1007/bf00040284

    Article  Google Scholar 

  • Matsuhiro B, Urzúa CC (1991) Agars from Chilean Gelidiaceae. Hydrobiologia 221:149–156. doi:10.1007/bf00028371

    Article  CAS  Google Scholar 

  • Melo RA (1998) Gelidium commercial exploitation: natural resources and cultivation. J Appl Phycol 10:303–314. doi:10.1023/A:1008070419158

    Article  Google Scholar 

  • Montecinos A, Broitman BR, Faugeron S, Haye PA, Tellier F, Guillemin ML (2012) Species replacement along a linear coastal habitat: phylogeography and speciation in the red alga Mazzaella laminarioides along the south east Pacific. BMC Evol Biol 12:97. doi:10.1186/1471-2148-12-97

    Article  Google Scholar 

  • Muhlin JF, Engel CR, Stessel R, Weatherbee RA, Brawley SH (2008) The influence of coastal topography, circulation patterns, and rafting in structuring populations of an intertidal alga. Mol Ecol 17:1198–1210. doi:10.1111/j.1365-294X.2007.03624.x

    Article  CAS  Google Scholar 

  • Neiva J, Assis J, Fernandes F, Pearson GA, Serrão EA, Maggs C (2014) Species distribution models and mitochondrial DNA phylogeography suggest an extensive biogeographical shift in the high-intertidal seaweed Pelvetia canaliculata. J Biogeogr 41:1137–1148. doi:10.1111/jbi.12278

    Article  Google Scholar 

  • Nelson WA, Farr TJ, Broom JES (2006) Phylogenetic diversity of New Zealand gelidiales as revealed by rbcL sequence data. J Appl Phycol 18:653–661. doi:10.1007/s10811-006-9068-0

    Article  Google Scholar 

  • Nikula R, Fraser CI, Spencer HG, Waters JM (2010) Circumpolar dispersal by rafting in two subantarctic kelp-dwelling crustaceans. Mar Ecol Prog Ser 405:221–230. doi:10.3354/meps08523

    Article  CAS  Google Scholar 

  • Nikula R, Spencer HG, Waters JM (2011a) Evolutionary consequences of microhabitat: population-genetic structuring in kelp- vs. rock-associated chitons. Mol Ecol 20:4915–4924. doi:10.1111/j.1365-294X.2011.05332.x

    Article  CAS  Google Scholar 

  • Nikula R, Spencer HG, Waters JM (2011b) Comparison of population-genetic structuring in congeneric kelp- versus rock-associated snails: a test of a dispersal-by-rafting hypothesis. Ecol Evol 1:169–180. doi:10.1002/ece3.16

    Article  Google Scholar 

  • Nikula R, Spencer HG, Waters JM (2013) Passive rafting is a powerful driver of transoceanic gene flow. Biol Lett 9:20120821. doi:10.1098/rsbl.2012.0821

    Article  Google Scholar 

  • Oliger P, Santelices B (1981) Physiological ecology studies on Chilean Gelidiales. J Exp Mar Biol Ecol 53:65–75. doi:10.1016/0022-0981(81)90084-8

    Article  Google Scholar 

  • Ortega M, Godínez-Ortega J, Garduño G (2001) Catálogo de algas bénticas de las costas mexicanas del Golfo de México y Mar Caribe. Instituto de Biología, Universidad Nacional Autónoma de México, México

    Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572. doi:10.1146/annurev.ecolsys.25.1.547

    Article  Google Scholar 

  • Perrone C, Felicini GP, Bottalico A (2006) The prostrate system of the Gelidiales: diagnostic and taxonomic importance. Bot Mar 49:23–33. doi:10.1515/Bot2006.003

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855. doi:10.1046/j.1523-1739.1998.96489.x

    Article  Google Scholar 

  • Piazzi L, Balata D, Bulleri F, Gennaro P, Ceccherelli G (2016) The invasion of Caulerpa cylindracea in the Mediterranean: the known, the unknown and the knowable. Mar Biol 163:161–174. doi:10.1007/S00227-016-2937-4

    Article  Google Scholar 

  • Polzin T, Daneshmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20. doi:10.1016/s0167-6377(02)00185-2

    Article  Google Scholar 

  • Ramírez M, Santelices B (1981) Análisis biogeográfico de la flora algológica de Antofagasta (norte de Chile). Bol Mus Nac Hist Nat Santiago de Chile 38:5–20

    Google Scholar 

  • Ramírez ME, Santelices B (1991) Catálogo de las algas marinas bentónicas de la costa temperada del Pacífico de Sudamérica. Monografías Biológicas 5, Ediciones Universidad Católica de Chile, Santiago de Chile

  • Robuchon M, Le Gall L, Mauger S, Valero M (2014) Contrasting genetic diversity patterns in two sister kelp species co-distributed along the coast of Brittany, France. Mol Ecol 23:2669–2685. doi:10.1111/mec.12774

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  Google Scholar 

  • Rojas R, León N, Rojas R (1996) Practical and descriptive techniques for Gelidium rex (Gelidiales, Rhodophyta) culture. Hydrobiologia 327:367–370

    Article  Google Scholar 

  • Sánchez R, Sepúlveda RD, Brante A, Cárdenas L (2011) Spatial pattern of genetic and morphological diversity in the direct developer Acanthina monodon (Gastropoda: Mollusca). Mar Ecol Prog Ser 434:121–131. doi:10.3354/meps09184

    Article  Google Scholar 

  • Santelices B (1980) Phytogeographic characterization of the temperate coast of Pacific South-America. Phycologia 19:1–12. doi:10.2216/i0031-8884-19-1-1.1

    Article  Google Scholar 

  • Santelices B (1986) The wild harvest and culture of the economically important species of Gelidium in Chile. In: Doty MS, Caddy JS, Santelices B (eds) Case of studies of seven commercial seaweed resources. FAO Fisheries Technical Paper, vol 281, FAO, Rome, pp 165–192

  • Santelices B (1990) New and old problems in the taxonomy of the Gelidiales (Rhodophyta). Hydrobiologia 204:125–135. doi:10.1007/bf00040224

    Article  Google Scholar 

  • Santelices B, Abbott IA (1985) Gelidium rex sp. nov. (Gelidiales. Rhodophyta) from central Chile. In: Abbott IA, Norris JN (eds) Taxonomy of economic seaweeds with reference to some Pacific and Caribbean species. California Sea Grant College Program, La Jolla, pp 33–36

    Google Scholar 

  • Santelices B, Montalva S (1983) Taxonomic studies on Gelidiaceae (Rhodophyta) from central Chile. Phycologia 22:185–196. doi:10.2216/i0031-8884-22-2-185.1

    Article  Google Scholar 

  • Santelices B, Stewart JG (1985) Pacific species of Gelidium Lamouroux and other Gelidiales (Rhodophyta), with keys and descriptions to the common or economically important species. In: Abbott IA, Norris JN (eds) Taxonomy of economic seaweeds with reference to some Pacific and Caribbean species. California Sea Grant College Program, California, La Jolla, pp 17–31

    Google Scholar 

  • Santelices B, Varela D (1994) Abiotic control of reattachment in Gelidium chilense (Montagne) Santelices and Montalva (Gelidiales, Rhodophyta). J Exp Mar Biol Ecol 177:145–155. doi:10.1016/0022-0981(94)90233-x

    Article  Google Scholar 

  • Santelices B, Aedo D, Hoffmann A (2002) Banks of microscopic forms and survival to darkness of propagules and microscopic stages of macroalgae. Rev Chil Hist Nat 75:547–555. doi:10.4067/S0716-078X2002000300006

    Article  Google Scholar 

  • Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos Trans R Soc Lond B Biol Sci 360:1879–1888. doi:10.1098/rstb.2005.1719

    Article  CAS  Google Scholar 

  • Selkoe KA, Toonen RJ (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Mar Ecol Prog Ser 436:291–305. doi:10.3354/meps09238

    Article  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279. doi:10.2307/2410134

    Article  Google Scholar 

  • Sosa P, García-Reina G (1992) Genetic variability and differentiation of sporophytes and gametophytes in populations of Gelidium arbuscula (Gelidiaceae: Rhodophyta) determined by isozyme electrophoresis. Mar Biol 113:679–688

    Article  CAS  Google Scholar 

  • Sosa PA, Valero M, Batista F, González-Pérez MA (1998) Genetic structure of natural populations of Gelidium species: a re-evaluation of results. J Appl Phycol 10:279–284. doi:10.1023/A:1008092023549

    Article  Google Scholar 

  • Soto EH, Báez P, Ramírez ME, Letelier S, Naretto J, Rebolledo A (2012) Biotopos marinos intermareales entre Canal Trinidad y Canal Smyth, Sur de Chile. Rev Biol Mar Oceanogr 47:177–191

    Article  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  Google Scholar 

  • Tapia FJ, Largier JL, Castillo M, Wieters EA, Navarrete SA (2014) Latitudinal discontinuity in thermal conditions along the nearshore of central-northern Chile. PLoS One 9:e110841. doi:10.1371/journal.pone.0110841

    Article  CAS  Google Scholar 

  • Technelysium Pty Ltd (2016) CHROMAS LITE. Available at: http://www.technelysium.com.au/chromas_lite.html. Accessed 12 April 2016

  • Tellier F, Meynard AP, Correa JA, Faugeron S, Valero M (2009) Phylogeographic analyses of the 30°S south-east Pacific biogeographic transition zone establish the occurrence of a sharp genetic discontinuity in the kelp Lessonia nigrescens: vicariance or parapatry? Mol Phylogenet Evol 53:679–693. doi:10.1016/j.ympev.2009.07.030

    Article  CAS  Google Scholar 

  • Tellier F, Vega JMA, Broitman BR, Vásquez JA, Valero M, Faugeron S (2011) The importance of having two species instead of one in kelp management: the Lessonia nigrescens species complex. Cah Biol Mar 52:455–465

    Google Scholar 

  • Thiel M, Gutow L (2005a) The ecology of rafting in the marine environment. I. The floating substrata. Oceanogr Mar Biol Ann Rev 42:181–263. doi:10.1201/9780203507810

    Google Scholar 

  • Thiel M, Gutow L (2005b) The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanogr Mar Biol Ann Rev 43:279–418. doi:10.1201/9781420037449

    Google Scholar 

  • Thiel M, Haye PA (2006) The ecology of rafting in the marine environment. III. Biogeographical and evolutionary consequences. Oceanogr Mar Biol Ann Rev 44:323–429. doi:10.1201/9781420006391.ch7

    Google Scholar 

  • Thiel M, Macaya EC, Acuña E, Arntz WE, Bastias H, Brokordt K, Camus PA, Castilla JC, Castro LR, Cortés M, Dumont CP, Escribano R, Fernández M, Gajardo JA, Gaymer CF, Gómez I, González AE, González HE, Haye PA, Illanes JE, Iriarte JL, Lancellotti DA, Luna-Jorquera G, Luxoroi C, Manríquez PH, Marín V, Muñoz P, Navarrete SA, Pérez E, Poulin E, Sellanes J, Sepúlveda HH, Stotz W, Tala F, Thomas A, Vargas CA, Vásquez JA, Vega JMA (2007) The Humboldt Current system of northern and central Chile. Oceanogr Mar Biol Ann Rev 45:195–344. doi:10.1201/9781420050943

    Google Scholar 

  • Thomas DT, Freshwater DW (2001) Studies of Costa Rican Gelidiales (Rhodophyta): four Caribbean taxa including Pterocladiella beachii sp nov. Phycologia 40:340–350. doi:10.2216/i0031-8884-40-4-340.1

    Article  Google Scholar 

  • Valero M, Destombe C, Mauger S, Ribout C, Engel CR, Daguin-Thiebaut C, Tellier F (2011) Using genetic tools for sustainable management of kelps: a literature review and the example of Laminaria digitata. Cah Biol Mar 52:467–483

    Google Scholar 

  • Vargas DR, Collado-Vides L (1996) Architectural models for apical patterns in Gelidium (Gelidiales, Rhodophyta): hypothesis of growth. Phycol Res 44:95–100

    Article  Google Scholar 

  • Vásquez JA, Vega JMA (2004) Ecosistemas marinos costeros del Parque Nacional Bosque Fray Jorge. In: Squeo F, Gutiérrez J, Hernández I (eds) Historia Natural del Parque Nacional Bosque Fray Jorge. Ediciones Universidad de La Serena, La Serena, pp 235–252

    Google Scholar 

  • Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc Natl Acad Sci USA 102:5432–5437. doi:10.1073/pnas.0501754102

    Article  CAS  Google Scholar 

  • Waters JM, Fraser CI, Hewitt GM (2013) Founder takes all: density-dependent processes structure biodiversity. Trends Ecol Evol 28:78–85. doi:10.1016/j.tree.2012.08.024

    Article  Google Scholar 

  • Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12. doi:10.3354/meps08287

    Article  Google Scholar 

  • Wichmann CS, Hinojosa IA, Thiel M (2012) Floating kelps in Patagonian Fjords: an important vehicle for rafting invertebrates and its relevance for biogeography. Mar Biol 159:2035–2049. doi:10.1007/s00227-012-1990-x

    Article  CAS  Google Scholar 

  • Yoon KJ, Kim KM, Boo GH, Miller KA, Boo SM (2014) Mitochondrial cox1 and cob sequence diversities in Gelidium vagum (Gelidiales, Rhodophyta) in Korea. Algae 29:15–25. doi:10.4490/algae.2014.29.1.015

    Article  CAS  Google Scholar 

  • Zakas C, Binford J, Navarrete SA, Wares JP (2009) Restricted gene flow in Chilean barnacles reflects an oceanographic and biogeographic transition zone. Mar Ecol Prog Ser 394:165–177. doi:10.3354/meps08265

    Article  Google Scholar 

Download references

Acknowledgements

This study was financed by the following grants: CONICYT/FONDECYT 1131082 to MT, F. Tala and F. Tellier, CONICYT/FONDECYT 1110437 to EM, and CONICYT/FONDECYT 11121504 to F. Tellier. BL received financial support by PhD-fellowship Beca CONICYT-PCHA/Doctorado Nacional/2014-21140010. Additional support came from International Research Network “Diversity, Evolution and Biotechnology of Marine Algae” (GDRI N ̊ 0803). The collaboration of Óscar Pino, José Pantoja, Alvaro Gallardo, Solange Pacheco, Ricardo Jeldres, María Fabiola Monsalvez, Ariel Cáceres, Ulyces Urtubia, Vieia Villalobos and Tim Kiessling in field activities is gratefully acknowledged. The valuable comments from two anonymous referees were very helpful in improving the original manuscript. We are grateful to Lucas Eastman for checking the language of the final manuscript.

Author information

Authors and Affiliations

  1. Doctorado en Biología y Ecología Aplicada, Universidad Católica del Norte, Coquimbo, Chile

    Boris A. López

  2. Departamento de Acuicultura y Recursos Agroalimentarios, Universidad de Los Lagos, Osorno, Chile

    Boris A. López

  3. Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Concepción, Chile

    Florence Tellier, Juan C. Retamal-Alarcón, Karla Pérez-Araneda & Ariel O. Fierro

  4. Centro de Investigación en Biodiversidad y Ambientes Sustentables (CIBAS), Universidad Católica de la Santísima Concepción, Concepción, Chile

    Florence Tellier & Karla Pérez-Araneda

  5. Laboratorio de Estudios Algales ALGALAB, Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

    Erasmo C. Macaya

  6. Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Coquimbo, Chile

    Erasmo C. Macaya & Martin Thiel

  7. Centro FONDAP de Investigaciones en Dinámica de Ecosistemas Marinos de Altas Latitudes (IDEAL), Valdivia, Chile

    Erasmo C. Macaya

  8. Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile

    Fadia Tala & Martin Thiel

  9. Centro de Investigación y Desarrollo Tecnológico en Algas (CIDTA), Universidad Católica del Norte, Coquimbo, Chile

    Fadia Tala

  10. Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Coquimbo, Chile

    Martin Thiel

Authors
  1. Boris A. López
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Florence Tellier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan C. Retamal-Alarcón
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karla Pérez-Araneda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ariel O. Fierro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Erasmo C. Macaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fadia Tala
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Martin Thiel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Florence Tellier.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interests.

Human and animals rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Responsibile Editor: O. Puebla.

Reviewed by Undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 286 kb)

Supplementary material 2 (PDF 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

López, B.A., Tellier, F., Retamal-Alarcón, J.C. et al. Phylogeography of two intertidal seaweeds, Gelidium lingulatum and G. rex (Rhodophyta: Gelidiales), along the South East Pacific: patterns explained by rafting dispersal?. Mar Biol 164, 188 (2017). https://doi.org/10.1007/s00227-017-3219-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3219-5

Search

Navigation