Genetic Affinities between Trans-Oceanic Populations of Non-Buoyant Macroalgae in the High Latitudes of the Southern Hemisphere

Marine biologists and biogeographers have long been puzzled by apparently non-dispersive coastal taxa that nonetheless have extensive transoceanic distributions. We here carried out a broad-scale phylogeographic study to test whether two widespread Southern Hemisphere species of non-buoyant littoral macroalgae are capable of long-distance dispersal. Samples were collected from along the coasts of southern Chile, New Zealand and several subAntarctic islands, with the focus on high latitude populations in the path of the Antarctic Circumpolar Current or West Wind Drift. We targeted two widespread littoral macroalgal species: the brown alga Adenocystisutricularis (Ectocarpales, Heterokontophyta) and the red alga Bostrychia intricata (Ceramiales, Rhodophyta). Phylogenetic analyses were performed using partial mitochondrial (COI), chloroplast (rbcL) and ribosomal nuclear (LSU / 28S) DNA sequence data. Numerous deeply-divergent clades were resolved across all markers in each of the target species, but close phylogenetic relationships – even shared haplotypes – were observed among some populations separated by large oceanic distances. Despite not being particularly buoyant, both Adenocystisutricularis and Bostrychia intricata thus show genetic signatures of recent dispersal across vast oceanic distances, presumably by attachment to floating substrata such as wood or buoyant macroalgae.

[1]  H. Spencer,et al.  Passive rafting is a powerful driver of transoceanic gene flow , 2013, Biology Letters.

[2]  G. Hewitt,et al.  Founder takes all: density-dependent processes structure biodiversity. , 2013, Trends in ecology & evolution.

[3]  J. Winston Dispersal in marine organisms without a pelagic larval phase. , 2012, Integrative and comparative biology.

[4]  C. Fraser,et al.  Poleward bound: biological impacts of Southern Hemisphere glaciation. , 2012, Trends in ecology & evolution.

[5]  F. Leliaert,et al.  Contrasting Geographical Distributions as a Result of Thermal Tolerance and Long-Distance Dispersal in Two Allegedly Widespread Tropical Brown Algae , 2012, PloS one.

[6]  C. Fraser The impacts of past climate change on sub-Antarctic nearshore ecosystems , 2012 .

[7]  G. Roderick,et al.  Long-distance dispersal: a framework for hypothesis testing. , 2012, Trends in Ecology & Evolution.

[8]  H. Spencer,et al.  Evolutionary consequences of microhabitat: population‐genetic structuring in kelp‐ vs. rock‐associated chitons , 2011, Molecular ecology.

[9]  H. Spencer,et al.  Comparison of population-genetic structuring in congeneric kelp- versus rock-associated snails: a test of a dispersal-by-rafting hypothesis , 2011, Ecology and evolution.

[10]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[11]  P. Arenas Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province , 2011 .

[12]  C. Fraser,et al.  Oceanic rafting by a coastal community , 2011, Proceedings of the Royal Society B: Biological Sciences.

[13]  E. Macaya,et al.  Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific , 2010 .

[14]  H. Spencer,et al.  Multigene phylogeny of the southern bull-kelp genus Durvillaea (Phaeophyceae: Fucales). , 2010, Molecular phylogenetics and evolution.

[15]  W. Nelson,et al.  Cladophoropsis brachyartra from southern South America is a synonym of Wittrockiella lyallii (Cladophorophyceae, Chlorophyta), previously regarded as endemic to New Zealand , 2010 .

[16]  C. Fraser,et al.  Asymmetric dispersal of southern bull‐kelp (Durvillaea antarctica) adults in coastal New Zealand: testing an oceanographic hypothesis , 2010, Molecular ecology.

[17]  E. Macaya,et al.  DNA BARCODING AND GENETIC DIVERGENCE IN THE GIANT KELP MACROCYSTIS (LAMINARIALES) 1 , 2010 .

[18]  C. Cruaud,et al.  A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the "brown algal crown radiation". , 2010, Molecular phylogenetics and evolution.

[19]  H. Spencer,et al.  Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp , 2010, BMC Evolutionary Biology.

[20]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[21]  H. Spencer,et al.  Circumpolar dispersal by rafting in two subantarctic kelp-dwelling crustaceans , 2010 .

[22]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[23]  C. Payri,et al.  TAXONOMIC REVISION OF SARGASSUM SPECIES (FUCALES, PHAEOPHYCEAE) FROM NEW CALEDONIA BASED ON MORPHOLOGICAL AND MOLECULAR ANALYSES 1 , 2009, Journal of phycology.

[24]  G. Saunders,et al.  On the utility of DNA barcoding for species differentiation among brown macroalgae (Phaeophyceae) including a novel extraction protocol , 2009 .

[25]  H. Spencer,et al.  Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum , 2009, Proceedings of the National Academy of Sciences.

[26]  J. West,et al.  Bostrychia (Rhodomelaceae, Rhodophyta) species of New Zealand, and relationships in the Southern Hemisphere , 2008 .

[27]  R. Weatherbee,et al.  The influence of coastal topography, circulation patterns, and rafting in structuring populations of an intertidal alga , 2008, Molecular ecology.

[28]  C. Lane,et al.  A MULTI‐GENE MOLECULAR INVESTIGATION OF THE KELP (LAMINARIALES, PHAEOPHYCEAE) SUPPORTS SUBSTANTIAL TAXONOMIC RE‐ORGANIZATION 1 , 2006 .

[29]  J. West,et al.  Molecular phylogeny of the subfamily Bostrychioideae (Ceramiales, Rhodophyta): subsuming Stictosiphonia and highlighting polyphyly in species of Bostrychia , 2006 .

[30]  C. Hoek The possible significance of long-range dispersal for the biogeography of seaweeds , 1987, Helgoländer Meeresuntersuchungen.

[31]  M. Thiel,et al.  The ecology of rafting in the marine environment. III. Biogeographical and evolutionary consequences , 2006 .

[32]  H. Spencer,et al.  CLADOGENESIS AS THE RESULT OF LONG‐DISTANCE RAFTING EVENTS IN SOUTH PACIFIC TOPSHELLS (GASTROPODA, TROCHIDAE) , 2005, Evolution; international journal of organic evolution.

[33]  M. Quartino,et al.  Biological and environmental characterization of marine macroalgal assemblages in Potter Cove, South Shetland Islands, Antarctica , 2005 .

[34]  M. Thiel,et al.  The Ecology of Rafting in the Marine Environment. II. The Rafting Organisms and Community , 2005 .

[35]  T. Ward,et al.  Marine introductions in the Shark Bay World Heritage Property, Western Australia: a preliminary assessment , 2005 .

[36]  M. Kimura A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[37]  B. Reviers,et al.  Morphology and taxonomy of Adenocystis longissima (Skottsberg) stat. nov. (Phaeophyceae) from subantarctic South America , 2004, Polar Biology.

[38]  J. West,et al.  Reproductive biology of Stictosiphonia hookeri (Rhodomelaceae, Rhodophyta) from Argentina, Chile, South Africa and Australia in laboratory culture , 1996, Hydrobiologia.

[39]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[40]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[41]  Stephen D. A. Smith Kelp rafts in the Southern Ocean , 2002 .

[42]  G. Saunders,et al.  MOLECULAR SYSTEMATICS OF THE FLORIDEOPHYCEAE (RHODOPHYTA) USING NUCLEAR LARGE AND SMALL SUBUNIT rDNA SEQUENCE DATA , 2001 .

[43]  J. West,et al.  Time-lapse videomicroscopy of cell (spore) movement in red algae , 2001 .

[44]  G. Saunders,et al.  The application of sequences of the ribosomal cistron to the systematics and classification of the florideophyte red algae (Florideophyceae, Rhodophyta) , 2001 .

[45]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[46]  G. Hewitt The genetic legacy of the Quaternary ice ages , 2000, Nature.

[47]  B. de Reviers,et al.  Adenocystaceae fam. nov. (Phaeophyceae) based on morphological and molecular evidence , 2000 .

[48]  T. J. Hilbish,et al.  Trans-Pacific range extension by rafting is inferred for the flat oyster Ostrea chilensis. , 1999, The Biological bulletin.

[49]  Karim Hodge,et al.  Over-water dispersal of lizards due to hurricanes , 1998, Nature.

[50]  Y. Fu,et al.  Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. , 1997, Genetics.

[51]  J. West,et al.  Physiological responses of the eulittoral macroalga Stictosiphonia hookeri (Rhodomelaceae, Rhodophyta) from Argentina and Chile: salinity, light and temperature acclimation , 1996 .

[52]  R. Veit,et al.  Long-distance dispersal of a subantarctic brooding bivalve (Gaimardia trapesina) by kelp-rafting , 1994 .

[53]  A. Peters,et al.  TEMPERATURE RESPONSES OF DISJUNCT TEMPERATE BROWN ALGAE INDICATE LONG‐DISTANCE DISPERSAL OF MICROTHALLI ACROSS THE TROPICS 1 , 1992 .

[54]  H. Harpending,et al.  Population growth makes waves in the distribution of pairwise genetic differences. , 1992, Molecular biology and evolution.

[55]  K. Johannesson The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? , 1988 .

[56]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[57]  D. Müller Culture studies on the life history of Adenocystis utricularis (Phaeophyceae, Dictyosiphonales) , 1984 .

[58]  R. Levins,et al.  Biogeography of the Puerto Rican Bank: Flotsam Transport of Terrestrial Animals , 1972 .