Abstract
The distribution of the Southern Ocean (SO) biota is the result of major geological, oceanographic, and climate changes during the last 50 million years (Ma). Several groups of marine benthic organisms exhibit marked taxonomic similarities between the Antarctic Peninsula and southern South America, where families, genera, and even species are currently co-distributed in these continents. Several species of macroalgae including Gigartina skottsbergii, Plocamium cartilagineum, and Iridaea cordata are currently found on both sides of the Drake Passage. Advances in molecular techniques have allowed estimating phylogenetic relationships, levels of differentiation and divergence time estimates between populations from these continents in order to determine whether they constitute separate evolutionary units. In this study, we determine whether Iridaea cordata represents the same evolutionary unit in southern South America and the Antarctic Peninsula or if populations on the two sides of the Drake Passage represent different genetic lineages. According to our results, I. cordata populations from the Antarctic Peninsula and South America are clearly distinguishable evolutionary units with 8.31% and 3.17% mtDNA and cpDNA molecular divergence, respectively. The separation between Antarctic and South American populations of I. cordata occurred at the end of the Miocene, between 5 Ma (rbcL) and 9 Ma (COI-5P). These results are similar to those reported in G. skottsbergii on both sides of the Drake Passage. Thus, I. cordata populations on the two sides of the Drake Passage should be considered two sister species. Cryptic speciation plays an important role in the evolution of the Southern Ocean; thus, the systematics, biogeography, and biodiversity of the region require major revisions.
Similar content being viewed by others
References
Allcock AL, Strugnell JM (2012) Southern Ocean diversity: new paradigms from molecular ecology. Trends Ecol Evol 27:520–528
Arntz WE (1999) Magellan—Antarctic: ecosystems that drifted apart. Summary Review. Sci Mar 63:503–511
Arntz WE, Thatje S, Gerdes D, Gili J-M, Gutt J, Jacob U, Montiel A, Orejas C, Teixidó N (2005) The Antarctic-Magellan connection: macrobenthos ecology on the shelf and upper slope, a progress report. Sci Mar 69:237–269
Aronson RB, Thatje S, Clarke A, Peck LS, Blake DB, Wilga CD, Seibel BA (2007) Climate change and invasibility of the Antarctic benthos. Annu Rev Ecol Evol Syst 38:129–154
Astorga-España MS, Mansilla A, Ojeda J, Marambio J, Rosenfeld S, Mendez F, Rodríguez JP, Ocaranza P (2017) Nutritional properties of dishes prepared with sub-Antarctic macroalgae—an opportunity for healthy eating. J Appl Phycol 29:2399–2406
Barnes DKA, Griffiths HJ, Kaiser S (2009) Geographic range shift responses to climate change by Antarctic benthos: where we should look. Mar Ecol Prog Ser 393:13–26
Billard E, Reyes J, Mansilla A, Faugeron S, Guillemin M-L (2015) Deep genetic divergence between austral populations of the red alga Gigartina skottsbergii reveals a cryptic species endemic to the Antarctic continent. Polar Biol 38:2021–2034
Bringloe TT, Saunders GW (2018) Mitochondrial DNA sequence data reveal the origins of postglacial marine macroalgal flora in the Northwest Atlantic. Mar Ecol Prog Ser 589:45–58
Buschmann A, Correa J, Westermeier R, Hernandez M, Norambuena R (2001) Red algal farming in Chile: a review. Aquaculture 194:203–220
Calderon MS, Boo SM (2016) Phylogeny of Phyllophoraceae (Rhodophyta, Gigartinales) reveals Asterfilopsis gen. nov. from the southern hemisphere. Phycologia 55:543–554
Clarke A (2008) Antarctic marine benthic diversity: patterns and processes. J Exp Mar Biol Ecol 366:48–55
Clarke A, Johnston IA (1996) Evolution and adaptive radiation of Antarctic fishes. Trends Ecol Evol 11:212–218
Clarke A, Barnes DKA, Hodgson DA (2005) How isolated is Antarctica? Trends Ecol Evol 20:004
Craigie JS (1990) Cell walls. In: Cole KM, Sheath RG (eds) Biology of the red algae. Cambridge University Press, Cambridge, pp 221–257
Crame JA (1999) An evolutionary perspective on marine faunal connections between southernmost South America and Antarctica. Sci Mar 63:1–14
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
Dalziel IWD, Lawver LA, Pearce JA, Barker PF, Hastie AR, Barfod DN, Schenke HW, Davis MB (2013) A potential barrier to deep Antarctic circumpolar flow until the late Miocene? Geology 41:947–950
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772
Dornburg A, Federman S, Eytan RI, Near TJ (2016) Cryptic species diversity in sub-Antarctic islands: a case study of Lepidonotothen. Mol Phylogenet Evol 104:32–43
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:1–19
Faugeron S, Valero M, Destombe C Martínez EA, Correa JA (2001) Hierarchical spatial structure and discriminant analysis of genetic diversity in the red alga Mazzaella laminarioides (Gigartinales, Rhodophyta). J Phycol 37:705–716
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Filatov DA (2009) Processing and population genetic analysis of multigenic datasets with ProSeq3 software. Bioinformatics 25:3189–3190
Fraser CI, Nikula R, Spencer HG, Waters JM (2009) Kelp genes reveal effects of subAntarctic sea ice during the Last Glacial Maximum. Proc Natl Acad Sci U S A 106:3249–3253
Fraser CI, Nikula R, Waters JM (2011) Oceanic rafting by a coastal community. Proc R Soc Lond B 278:649–655
Fraser CI, Zuccarello GC, Spencer HG, Salvatore LC, Garcia GR, Waters JM (2013) Genetic affinities between trans-oceanic populations of non-buoyant macroalgae in the high latitudes of the Southern Hemisphere. PLoS One 8:e69138
Fraser CI, Kay GM, du Plessis M, Ryan PG (2017) Breaking down the barrier: dispersal across the Antarctic polar front. Ecography 40:235–237
Fraser CI, Morrison AK, Hogg AMC, Macaya EC, van Sebille E, Ryan PG, Padovan A, Jack C, Valdivia N, Waters JM (2018) Antarctica’s ecological isolation will be broken by storm-driven dispersal warming. Nat Clim Chang 8:704–708
González-Wevar CA, Hüne M, Segovia NI, Nakano T, Spencer HG, Chown SL, Saucède T, Johnstone G, Mansilla A, Poulin E (2017) Following the Antarctic Circumpolar Current: patterns and processes in the biogeography of the limpet Nacella (Mollusca: Patellogastropoda) across the Southern Ocean. J Biogeogr 44:861–874
González-Wevar CA, Segovia NI, Rosenfeld S, Ojeda J, Hüne M, Naretto J, Saudède T, Brickle P, Morley S, Féral JP et al (2018) Unexpected absence of island endemics: long-distance dispersal in higher latitude sub-Antarctic Siphonaria (Gastropoda: Euthyneura) species. J Biogeogr 45:874–884
Guillemin ML, Contreras-Porcia L, Ramírez ME, Macaya EC, Bulboa Contador C, Woods H, Wyatt C, Brodie J (2016a) The bladed Bangiales (Rhodophyta) of the South Eastern Pacific: molecular species delimitation reveals extensive diversity. Mol Phylogenet Evol 94:814–826
Guillemin ML, Valero M, Tellier F, Macaya EC, Destombe C, Faugeron S (2016b) Phylogeography of seaweeds in the South East Pacific: complex evolutionary processes along a latitudinal gradient. In: Hu ZM, Fraser C (eds) Seaweed Phylogeography. Springer, Dordrecht, pp 251–277
Guillemin ML, Dubrasquet H, Reyes J, Valero M (2018) Comparative phylogeography of six red algae along the Antarctic peninsula: extreme genetic depletion linked to historical bottlenecks and recent expansion. Polar Biol 41:827–837
Hansen JE (1977) Ecology and natural history of Iridaea cordata (Gigartinales, Rhodophyta) growth. J Phycol 13:395–402
Heinrich S, Zonneveld KAF, Bickert T, Willems H (2011) The Benguela upwelling related to the Miocene cooling events and the development of the Antarctic Circumpolar Current: evidence from calcareous dinoflagellate cysts. Paleoceanography 26:PA3209
Held C, Wägele J-W (2005) Cryptic speciation within the widespread Antartic crustacean Cerotoserolis trilobitoides (Crustacea, Isopoda). In: Huiskes AHL, Gieskes WWC, Rozema RML, Schorno SM, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys, Leiden, pp 305–309
Hommersand MH, Fredericq S, Freshwater DW (1994) Phylogenetic systematics and biogeography of the Gigartinaceae (Gigartinales, Rhodophyta) based on sequence analysis of rbcL. Bot Mar 37:193–203
Hommersand MH, Fredericq S, Freshwater DW, Hughey J (1999) Recent developments in the systematics of the Gigartinaceae (Gigartinales, Rhodophyta) based on rbcL sequence analysis and morphological evidence. Phycol Res 47:139–151
Hommersand MH, Fredericq S (2003) Biogeography of the marine red algae of the South African West Coast: a molecular approach. Proceedings XVIIth International Seaweed Symposium, Oxford University Press, pp. 325–336
Hommersand MH, Moe RL, Amsler CD, Fredericq S (2009) Notes on the systematics and biogeographical relationships of Antarctic and sub-Antarctic Rhodophyta with descriptions of four new genera and five new species. Bot Mar 52:509–534
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Ji Y, Xu Z, Zou D, Gao K (2016) Ecophysiological responses of marine macroalgae to climate change factors. J Appl Phycol 28:2953–2967
Kamiya M, Zuccarello GC, West JA (2004) Phylogeography of Caloglossa leprieurii and related species (Delesseriaceae, Rhodophyta) based on the rbcL gene sequences. Jpn J Phycol 52:147–151
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Le Gall L, Saunders GW (2010) DNA barcoding is a powerful tool to uncover algal diversity: a case study of the Phyllophoraceae (Gigartinales, Rhodophyta) in the Canadian flora. J Phycol 46:374–389
Lewis AR, Marchant DR, Ashworth AC, Hedenäs L, Hemming SR, Johnson JV, Leng MJ, Machlus ML, Newton AE, Raine JI et al (2008) Mid-Miocene cooling and the extinction of tundra in continental Antarctica. Proc Natl Acad Sci U S A 105:10676–10680
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lin S, Fredericq S, Hommersand MH (2001) Systematics of the Delesseriaceae (Ceramiales, Rhodophyta) based on large subunit rDNA and rbcL sequences, including the Phycodryoideae, subfam, Nov. J Geophys Res 37:881–899
Linse K, Griffiths HJ, Barnes DKA, Clarke A (2006) Biodiversity and biogeography of Antarctic and sub-Antarctic mollusca. Deep-Sea Res 53:985–1008
Livermore R, Nankivell A, Eagles G, Morris P (2005) Paleogene opening of Drake Passage. Earth Planet Sci Lett 236:459–470
Macaya EC, Zuccarello GC (2010) DNA barcoding and genetic divergence in the giant kelp Macrocystis (Laminariales). J Phycol 46:736–742
Mansilla A, Ávila M, Yokoya NS (2012) Current knowledge on biotechnological interesting seaweeds from the Magallanes region, Chile. Rev Bras 22:760–767
Martínez EA, Cárdenas L, Pinto R (2003) Recovery and genetic diversity of the intertidal kelp Lessonia nigrescens (Phaeophyceae) 20 years after El Niño 1982/83. J Phycol 39:504–508
Moon KL, Chown SL, Fraser CI (2017) Reconsidering connectivity in the sub-Antarctic. Biol Rev 92:2164–2181
Near TJ, Dornburg A, Kuhn KL, Eastman JT, Pennington JN, Paternello T, Zane L, Fernández DA, Jones CD (2012) Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc Natl Acad Sci U S A 109:3434–3439
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
Page TJ, Linse K (2002) More evidence of speciation and dispersal across Antarctic Polar Front through molecular systematics of Southern Ocean Limatula (Bivalvia: Limidae). Polar Biol 25:818–826
Patarnello T, Bargelloni L, Varotto V, Battaglia B (1996) Krill evolution and the Antarctic Ocean currents: evidence of vicariant speciation as inferred by molecular data. Mar Biol 126:603–608
Pfuh HA, McCave IN (2005) Evidence for late Oligocene establishment of the Antarctic Circumpolar Current. Earth Planet Sci Lett 235:715–728
Poulin E, González-Wevar C, Díaz A, Gerard K, Hüne M (2014) Divergence between Antarctic and South American marine invertebrates: what molecular biology tells us about Scotia Arc geodynamics and the intensification of the Antarctic Circumpolar Current. Glob Planet Chang 123:392–399
Rintoul SR, Hughes C, Olbers D (2001) The Antarctic Circumpolar Current system. In: Siedler G, Church J, Gould J (eds) Ocean circulation and climate. New York Academic Press, New York, pp 271–302
Robuchon M, Valero M, Gey D, Le Gall L (2015) How does molecular-assisted identification affect our estimation of α, β, and γ biodiversity? An example from understory red seaweeds (Rhodophyta) of Laminaria kelp forests in Brittany, France. Genetica 143:207–223. https://doi.org/10.1007/s10709-014-9796-z
Salzburger W, Ewing GB, Von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 20:1952–1963
Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos Trans R Soc B 360:1879–1888
Sérsic AN, Cosacov A, Cocucci AA, Johnson LA, Pozner R, Avila LJ, Sites JW Jr, Morando M (2011) Emerging phylogeographical patterns of plants and terrestrial vertebrates from Patagonia. Biol J Linn Soc 103:475–494
Shevenell AE, Kennett JP, Lea DW (2004) Middle Miocene Southern Ocean cooling and Antarctic cryosphere expansion. Science 305:1766–1770
Silberfeld T, Leigh JW, Verbruggen H, Cruaud C, de Reviers B, Rousseau F (2010) A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the “brown algal crown radiation”. Mol Phylogenet Evol 56:659–674
Valdenegro A, Silva N (2003) Caracterización oceanográfica física y química de la zona de canales y fiordos australes de Chile entre el Estrecho de Magallanes y Cabo de Hornos (CIMAR 3 Fiordos). Revista Ciencia y Tecnología del Mar 26:19–60
Verducci M, Foresi LM, Scott GH, Sprovieri M, Lirer F, Pelosi N (2009) The Middle Miocene climatic transition in the Southern Ocean: evidence of paleoclimatic and hydrographic changes at Kerguelen plateau from planktonic foraminifers and stable isotopes. Palaeogeogr Palaeoclimatol Palaeoecol 280:371–386
Vianna JA, Medina-Vogel G, Chehébar C, Sielfeld W, Olavarría C, Faugeron S (2011) Phylogeography of the Patagonian otter Lontra provocax: adaptive divergence to marine habitat or signature of southern glacial refugia? BMC Evol Biol 11:53
Wiencke C (1990) Seasonality of red and green macroalgae from Antarctica—a long-term culture study under fluctuating Antarctic daylengths. Polar Biol 10:601–607
Wiencke C, Amsler CD (2012) Seaweeds and their communities. In: Bischof K, Wiencke C (eds) Polar Regions, Seaweed biology: novel insights into ecophysiology, ecology and utilization. Springer, Berlin, pp 265–291
Wiencke C, Amsler CD, Clayton MN (2014) Macroalgae. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C et al (eds) Biogeographic atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 66–73
Wilson NG, Schrödl M, Halanych KM (2009) Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia). Mol Ecol 18:965–984
Wright F (1990) The 'effective number of codons' used in a gene. Gene 87:23-29. https://doi.org/10.1016/0378-1119(90)90491-9
Xia X, Xie Z (2001) DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92:371–373
Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693
Zemlak TS, Habit EM, Walde SJ, Carrea C, Ruzzante DE (2010) Surviving historical Patagonian landscapes and climate: molecular insights from Galaxias maculatus. BMC Evol Biol 10:67
Funding
This study was supported by different projects and institutions: INACH project MG_07-17 to P.O-B; Fondecyt Initiation project 11140087, INACH RG_18-17, and GAB (ACT172065) to C.A.G-W; projects P05-002 ICM and PFB023 (Instituto de Ecología y Biodiversidad IEB) to C.A.G-W. and A.M.; Fondecyt Regular project 1140940 to A.M. and P.O-B.; INACH project RG_15-16 to M-L. G.; and FONDAP program project no. 15150003 to M-L.G. and C.A.G-W.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Ocaranza-Barrera, P., González-Wevar, C.A., Guillemin, ML. et al. Molecular divergence between Iridaea cordata (Turner) Bory de Saint-Vincent from the Antarctic Peninsula and the Magellan Region. J Appl Phycol 31, 939–949 (2019). https://doi.org/10.1007/s10811-018-1656-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-018-1656-2