Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Genetic differentiation between estuarine and open coast ecotypes of a dominant ecosystem engineer

M. A. Coleman A B E , J. S. Clark C , M. A. Doblin C , M. J. Bishop D and B. P. Kelaher B
+ Author Affiliations
- Author Affiliations

A Department of Primary Industries, NSW Fisheries, PO Box 4321, Coffs Harbour, NSW 2450, Australia.

B National Marine Science Centre, Southern Cross University, 2 Bay Drive, Coffs Harbour, NSW 2350, Australia.

C Climate Change Cluster (C3), University of Technology Sydney, PO Box 123, Broadway, NSW 2007, Australia.

D Department of Biological Sciences, Macquarie University, NSW 2109, Australia.

E Corresponding author. Email: melinda.coleman@gmail.com

Marine and Freshwater Research 70(7) 977-985 https://doi.org/10.1071/MF17392
Submitted: 22 December 2017  Accepted: 28 June 2018   Published: 18 September 2018

Abstract

Temperate intertidal shores globally are often dominated by habitat-forming seaweeds, but our knowledge of these systems is heavily biased towards northern hemisphere species. Rocky intertidal shores throughout Australia and New Zealand are dominated by a single monotypic species, Hormosira banksii. This species plays a key role in facilitating biodiversity on both rocky shores and estuarine habitats, yet we know little about the processes that structure populations. Herein we characterise the genetic diversity and structure of Hormosira and demonstrate strong restrictions to gene flow over small spatial scales, as well as between estuarine and open coast populations. Estuarine ecotypes were often genetically unique from nearby open coast populations, possibly due to extant reduced gene flow between habitats, founder effects and coastal geomorphology. Deviations from random mating in many locations suggest complex demographic processes are at play within shores, including clonality in estuarine populations. Strong isolation by distance in Hormosira suggests that spatial management of intertidal habitats will necessitate a network of broad-scale protection. Understanding patterns of genetic diversity and gene flow in this important ecosystem engineer will enhance the ability to manage, conserve and restore this key species into the future.

Additional keywords: asexual, clonality, diversity, foundation species, gene flow, Hormosira banksii, intertidal.


References

Arnaud‐Haond, S., Duarte, C. M., Alberto, F., and Serrao, E. A. (2007). Standardizing methods to address clonality in population studies. Molecular Ecology 16, 5115–5139.
Standardizing methods to address clonality in population studies.Crossref | GoogleScholarGoogle Scholar |

Bellgrove, A., Clayton, M. N., and Quinn, G. P. (1997). Effects of secondarily treated sewage effluent on intertidal macroalgal recruitment processes. Marine and Freshwater Research 48, 137–146.
Effects of secondarily treated sewage effluent on intertidal macroalgal recruitment processes.Crossref | GoogleScholarGoogle Scholar |

Bellgrove, A., McKenzie, P. F., McKenzie, J. L., and Sfiligoj, B. J. (2010). Restoration of the habitat-forming fucoid alga Hormosira banksii at effluent-affected sites: competitive exclusion by coralline turfs. Marine Ecology Progress Series 419, 47–56.
Restoration of the habitat-forming fucoid alga Hormosira banksii at effluent-affected sites: competitive exclusion by coralline turfs.Crossref | GoogleScholarGoogle Scholar |

Bellgrove, A., McKenzie, P. F., Cameron, H., and Pocklington, J. B. (2017). Restoring rocky intertidal communities: lessons from a benthic macroalgal ecosystem engineer. Marine Pollution Bulletin 117, 17–27.
Restoring rocky intertidal communities: lessons from a benthic macroalgal ecosystem engineer.Crossref | GoogleScholarGoogle Scholar |

Berry, O., Tocher, M. D., and Sarre, S. D. (2004). Can assignment tests measure dispersal? Molecular Ecology 13, 551–561.
Can assignment tests measure dispersal?Crossref | GoogleScholarGoogle Scholar |

Bertness, M. D., and Leonard, G. H. (1997). The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78, 1976–1989.
The role of positive interactions in communities: lessons from intertidal habitats.Crossref | GoogleScholarGoogle Scholar |

Bishop, M. J., Morgan, T., Coleman, M. A., Kelaher, B. P., Hardstaff, L. K., and Evenden, R. W. (2009). Facilitation of molluscan assemblages in mangroves by the fucalean alga Hormosira banksii. Marine Ecology Progress Series 392, 111–122.
Facilitation of molluscan assemblages in mangroves by the fucalean alga Hormosira banksii.Crossref | GoogleScholarGoogle Scholar |

Bishop, M. J., Byers, J. E., Marcek, B. J., and Gribben, P. E. (2012). Density-dependent facilitation cascades determine epifaunal community structure in temperate Australian mangroves. Ecology 93, 1388–1401.
Density-dependent facilitation cascades determine epifaunal community structure in temperate Australian mangroves.Crossref | GoogleScholarGoogle Scholar |

Bishop, M. J., Fraser, J., and Gribben, P. E. (2013). Morphological traits and density of foundation species modulate a facilitation cascade in Australian mangroves. Ecology 94, 1927–1936.
Morphological traits and density of foundation species modulate a facilitation cascade in Australian mangroves.Crossref | GoogleScholarGoogle Scholar |

Bohonak, A. J. (2002). IBD (Isolation by Distance): a program for analyses of isolation by distance. The Journal of Heredity 93, 153–154.
IBD (Isolation by Distance): a program for analyses of isolation by distance.Crossref | GoogleScholarGoogle Scholar |

Brawley, S. H., and Johnson, L. E. (1993). Predicting desiccation stress in microscopic organisms. The use of agarose beads to determine evaporation within and between intertidal microhabitats. Journal of Phycology 29, 528–535.
Predicting desiccation stress in microscopic organisms. The use of agarose beads to determine evaporation within and between intertidal microhabitats.Crossref | GoogleScholarGoogle Scholar |

Browning, S. A., and Goodwin, I. D. (2013). Large-scale influences on the evolution of winter subtropical maritime cyclones affecting Australia’s east coast. Monthly Weather Review 141, 2416–2431.
Large-scale influences on the evolution of winter subtropical maritime cyclones affecting Australia’s east coast.Crossref | GoogleScholarGoogle Scholar |

Campbell, A. H., Marzinelli, E. M., Verges, A., Coleman, M. A., and Steinberg, P. D. (2014). Towards restoration of missing underwater forests. PLoS One 9, e84106.
Towards restoration of missing underwater forests.Crossref | GoogleScholarGoogle Scholar |

Clark, J. S. (2016) Assessing the vulnerability of a habitat forming macroalga to climate warming: roles of physiology, ecology and evolutionary processes in determining resilience. Ph.D. Thesis, University of Technology, Sydney, Sydney, NSW, Australia.

Clarke, S. M., and Womersley, H. B. S. (1981). Cross-fertilization and hybrid development of forms of the brown alga Hormosira banksii (Turner) Decaisne. Australian Journal of Botany 29, 497–505.
Cross-fertilization and hybrid development of forms of the brown alga Hormosira banksii (Turner) Decaisne.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A. (2013). Connectivity of the habitat-forming kelp, Ecklonia radiata within and among estuaries and open coast. PLoS One 8, e64667.
Connectivity of the habitat-forming kelp, Ecklonia radiata within and among estuaries and open coast.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., and Brawley, S. H. (2005a). Are life history characteristics good predictors of genetic diversity and structure? A case study of the intertidal alga Fucus spiralis (Heterokontophyta; Phaeophyceae). Journal of Phycology 41, 753–762.
Are life history characteristics good predictors of genetic diversity and structure? A case study of the intertidal alga Fucus spiralis (Heterokontophyta; Phaeophyceae).Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., and Brawley, S. H. (2005b). Spatial and temporal variability in dispersal and population genetic structure of a rockpool alga. Marine Ecology Progress Series 300, 63–77.
Spatial and temporal variability in dispersal and population genetic structure of a rockpool alga.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., and Kelaher, B. P. (2009). Connectivity among fragmented populations of a habitat-forming alga, Phyllospora comosa (Phaeophyceae, Fucales) on an urbanised coast. Marine Ecology Progress Series 381, 63–70.
Connectivity among fragmented populations of a habitat-forming alga, Phyllospora comosa (Phaeophyceae, Fucales) on an urbanised coast.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., and Wernberg, T. (2017). Forgotten underwater forests: the key role of fucoids on Australian temperate reefs. Ecology and Evolution 7, 8406–8418.
Forgotten underwater forests: the key role of fucoids on Australian temperate reefs.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., and Wernberg, T. (2018). Genetic and morphological diversity in sympatric sexual and asexual kelp ecotypes. Aquatic Biology 27, 65–73.
Genetic and morphological diversity in sympatric sexual and asexual kelp ecotypes.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., Gillanders, B. M., and Connell, S. D. (2009). Dispersal and gene flow in the habitat-forming kelp, Ecklonia radiata: relative degrees of isolation across an east–west coastline. Marine and Freshwater Research 60, 802–809.
Dispersal and gene flow in the habitat-forming kelp, Ecklonia radiata: relative degrees of isolation across an east–west coastline.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., Chambers, J., Knott, N. A., Malcolm, H. A., Harasti, D., Jordan, A., and Kelaher, B. P. (2011a). Connectivity within and among a network of temperate marine reserves. PLoS One 6, e20168.
Connectivity within and among a network of temperate marine reserves.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., Roughan, M., Macdonald, H. S., Connell, S. D., Gillanders, B. M., Kelaher, B. P., and Steinberg, P. D. (2011b). Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp. Journal of Ecology 99, 1026–1032.
Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp.Crossref | GoogleScholarGoogle Scholar |

Coleman, M. A., Feng, M., Roughan, M., Cetina-Heredia, P., and Connell, S. D. (2013). Temperate shelf water dispersal by Australian boundary currents: implications for population connectivity. Limnology and Oceanography: Fluids and Environments 3, 295–309.

Cornuet, J.-M., Piry, S., Luikart, G., Estoup, A., and Solignac, M. (1999). New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153, 1989–2000.

Coyer, J. A., Peters, A. F., Stam, W. T., and Olsen, J. L. (2003). Post-ice age recolonization and differentiation of Fucus serratus L. (Phaeophyceae; Fucaceae) populations in Northern Europe. Molecular Ecology 12, 1817–1829.
Post-ice age recolonization and differentiation of Fucus serratus L. (Phaeophyceae; Fucaceae) populations in Northern Europe.Crossref | GoogleScholarGoogle Scholar |

Doblin, M. A., and Clayton, M. N. (1995). Effects of secondarily treated sewage effluent on the early life-history stages of two species of brown macroalgae: Hormosira banksii and Durvillaea potatorum. Marine Biology 122, 689–698.
Effects of secondarily treated sewage effluent on the early life-history stages of two species of brown macroalgae: Hormosira banksii and Durvillaea potatorum.Crossref | GoogleScholarGoogle Scholar |

Durrant, H. M. S., Burridge, C. P., Kelaher, B. P., Barrett, N. S., Edgar, G. J., and Coleman, M. A. (2014). Implications of macroalgal isolation by distance for networks of marine protected areas. Conservation Biology 28, 438–445.
Implications of macroalgal isolation by distance for networks of marine protected areas.Crossref | GoogleScholarGoogle Scholar |

Engel, C. R., Daguin, C., and Serrao, E. A. (2005). Genetic entities and mating system in hermaphroditic Fucus spiralis and its close dioecious relative F. vesiculosus (Fucaceae, Phaeophyceae). Molecular Ecology 14, 2033–2046.
Genetic entities and mating system in hermaphroditic Fucus spiralis and its close dioecious relative F. vesiculosus (Fucaceae, Phaeophyceae).Crossref | GoogleScholarGoogle Scholar |

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software structure: a simulation study.Crossref | GoogleScholarGoogle Scholar |

Excoffier, L., Laval, G., and Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.
Arlequin (version 3.0): an integrated software package for population genetics data analysis.Crossref | GoogleScholarGoogle Scholar |

Fairweather, P. G. (1990). Sewage and the biota on seashores: assessment of impact in relation to natural variability. Environmental Monitoring and Assessment 14, 197–210.
Sewage and the biota on seashores: assessment of impact in relation to natural variability.Crossref | GoogleScholarGoogle Scholar |

Goudet, J. (1995). FSTAT (version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
FSTAT (version 1.2): a computer program to calculate F-statistics.Crossref | GoogleScholarGoogle Scholar |

Hay, M. E. (1981). The functional morphology of turf-forming seaweeds: persistence in stressful marine habitats. Ecology 62, 739–750.
The functional morphology of turf-forming seaweeds: persistence in stressful marine habitats.Crossref | GoogleScholarGoogle Scholar |

Jakobsson, M., and Rosenberg, N. A. (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.Crossref | GoogleScholarGoogle Scholar |

Jenkins, S. R., Hawkins, S. J., and Norton, T. A. (1999). Direct and indirect effects of a macroalgal canopy and limpet grazing in structuring a sheltered inter-tidal community. Marine Ecology Progress Series 188, 81–92.
Direct and indirect effects of a macroalgal canopy and limpet grazing in structuring a sheltered inter-tidal community.Crossref | GoogleScholarGoogle Scholar |

Johannesson, K., Johansson, D., Larsson, K. H., Huenchuñir, C. J., Perus, J., Forslund, H., Kautsky, L., and Pereyra, R. T. (2011). Frequent clonality in fucoids (Fucus radicans and Fucus vesiculosus; Fucales, Phaeophyceae) in the Baltic Sea. Journal of Phycology 47, 990–998.
Frequent clonality in fucoids (Fucus radicans and Fucus vesiculosus; Fucales, Phaeophyceae) in the Baltic Sea.Crossref | GoogleScholarGoogle Scholar |

Kain, J. M. (2015). Hormosira banksii (Phaeophyceae): a tough survivor in the harsh conditions of high intertidal pools in southeast Australia. European Journal of Phycology 50, 408–421.
Hormosira banksii (Phaeophyceae): a tough survivor in the harsh conditions of high intertidal pools in southeast Australia.Crossref | GoogleScholarGoogle Scholar |

Keough, M. J., and Quinn, G. P. (1998). Effects of periodic disturbances from trampling on rocky intertidal algal beds. Ecological Applications 8, 141–161.

King, R. J. (1981). The free-living Hormosira banksii (Turner) Decaisne associated with mangroves in temperate eastern Australia. Botanica Marina 24, 256–273.
The free-living Hormosira banksii (Turner) Decaisne associated with mangroves in temperate eastern Australia.Crossref | GoogleScholarGoogle Scholar |

King, R. J., and Wheeler, M. (1985). Composition and geographic distribution of mangrove macroalgal communities in New South Wales. Proceedings of the Linnean Society of New South Wales 108, 97–117.

Levring, T. (1949). Fertilization experiments with Horinosira banksii (Tnrn.) Dcne. Physiologia Plantarum 2, 45–55.
Fertilization experiments with Horinosira banksii (Tnrn.) Dcne.Crossref | GoogleScholarGoogle Scholar |

Lilley, S. A., and Schiel, D. R. (2006). Community effects following the deletion of a habitat-forming alga from rocky marine shores. Oecologia 148, 672–681.
Community effects following the deletion of a habitat-forming alga from rocky marine shores.Crossref | GoogleScholarGoogle Scholar |

Macinnis-Ng, C. M. O., Morrison, D. A., and Ralph, P. J. (2005). Temporal and spatial variation in the morphology of the brown macroalga Hormosira banksii (Fucales, Phaeophyta). Botanica Marina 48, 198–202.
Temporal and spatial variation in the morphology of the brown macroalga Hormosira banksii (Fucales, Phaeophyta).Crossref | GoogleScholarGoogle Scholar |

Martínez, B., Wernberg, T., Radford, B., Thomsen, M. S., Russell, B. D., Connell, S. D., Bradshaw, C. J. A., Carreño, F., Fordham, D. A., and Gurgel, C. F. D. (in press). Predictions of responses to ocean warming for habitat-forming seaweeds. Diversity & Distributions , .
Predictions of responses to ocean warming for habitat-forming seaweeds.Crossref | GoogleScholarGoogle Scholar |

McKenzie, P. F., and Bellgrove, A. (2008). Dispersal of Hormosira banksii (Phaeophyceae) via detached fragments: reproductive viability and longevity. Journal of Phycology 44, 1108–1115.
Dispersal of Hormosira banksii (Phaeophyceae) via detached fragments: reproductive viability and longevity.Crossref | GoogleScholarGoogle Scholar |

Millar, A., and Kraft, G. (1994). Catalogue of marine brown algae (Phaeophyta) of New South Wales, including Lord Howe Island, south-western Pacific. Australian Systematic Botany 7, 1–47.
Catalogue of marine brown algae (Phaeophyta) of New South Wales, including Lord Howe Island, south-western Pacific.Crossref | GoogleScholarGoogle Scholar |

Mueller, R., Fischer, A. M., Bolch, C. J. S., and Wright, J. T. (2015). Environmental correlates of phenotypic variation: do variable tidal regimes influence morphology in intertidal seaweeds? Journal of Phycology 51, 859–871.
Environmental correlates of phenotypic variation: do variable tidal regimes influence morphology in intertidal seaweeds?Crossref | GoogleScholarGoogle Scholar |

Muhlin, J. F., Engel, C. R., Stessel, R., Weatherbee, R. A., and Brawley, S. H. (2008). The influence of coastal topography, circulation patterns, and rafting in structuring populations of an intertidal alga. Molecular Ecology 17, 1198–1210.
The influence of coastal topography, circulation patterns, and rafting in structuring populations of an intertidal alga.Crossref | GoogleScholarGoogle Scholar |

Neiva, J., Pearson, G. A., Valero, M., and Serrão, E. A. (2012). Fine-scale genetic breaks driven by historical range dynamics and ongoing density-barrier effects in the estuarine seaweed Fucus ceranoides L. BMC Evolutionary Biology 12, 78.
Fine-scale genetic breaks driven by historical range dynamics and ongoing density-barrier effects in the estuarine seaweed Fucus ceranoides L.Crossref | GoogleScholarGoogle Scholar |

Osborn, J. E. (1948). The structure and life history of Hormosira banksii (Turner) Decaisne. Transactions of the Royal Society of New Zealand 77, 47–71.

Pearson, G. A., and Serrão, E. A. (2006). Revisiting synchronous gamete release by fucoid algae in the intertidal zone: fertilization success and beyond? Integrative and Comparative Biology 46, 587–597.
Revisiting synchronous gamete release by fucoid algae in the intertidal zone: fertilization success and beyond?Crossref | GoogleScholarGoogle Scholar |

Piry, S., Alapetite, A., Cornuet, J. M., Paetkau, D., Baudouin, L., and Estoup, A. (2004). GENECLASS2: a software for genetic assignment and first-generation migrant detection. The Journal of Heredity 95, 536–539.
GENECLASS2: a software for genetic assignment and first-generation migrant detection.Crossref | GoogleScholarGoogle Scholar |

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

Putman, A. I., and Carbone, I. (2014). Challenges in analysis and interpretation of microsatellite data for population genetic studies. Ecology and Evolution 4, 4399–4428.

Ralph, P. J., Morrison, D. A., and Addison, A. (1998). A quantitative study of the patterns of morphological variation within Hormosira banksii (Turner) Decaisne (Fucales: Phaeophyta) in south-eastern Australia. Journal of Experimental Marine Biology and Ecology 225, 285–300.
A quantitative study of the patterns of morphological variation within Hormosira banksii (Turner) Decaisne (Fucales: Phaeophyta) in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Rannala, B., and Mountain, J. L. (1997). Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America 94, 9197–9201.
Detecting immigration by using multilocus genotypes.Crossref | GoogleScholarGoogle Scholar |

Rosenberg, N. A. (2004). distruct: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.
distruct: a program for the graphical display of population structure.Crossref | GoogleScholarGoogle Scholar |

Rousset, F. (1997). Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228.

Schiel, D. R., and Lilley, S. A. (2007). Gradients of disturbance to an algal canopy and the modification of an intertidal community. Marine Ecology Progress Series 339, 1–11.
Gradients of disturbance to an algal canopy and the modification of an intertidal community.Crossref | GoogleScholarGoogle Scholar |

Schiel, D. R., and Taylor, D. I. (1999). Effects of trampling on a rocky intertidal algal assemblage in southern New Zealand. Journal of Experimental Marine Biology and Ecology 235, 213–235.
Effects of trampling on a rocky intertidal algal assemblage in southern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Tatarenkov, A., Bergström, L., Jönsson, R. B., Serrão, E. A., Kautsky, L., and Johannesson, K. (2005). Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus. Molecular Ecology 14, 647–651.
Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus.Crossref | GoogleScholarGoogle Scholar |

Teixeira, S., Pearson, G. A., Candeias, R., Madeira, C., Valero, M., and Serrão, E. A. (2016). Lack of fine-scale genetic structure and distant mating in natural populations of Fucus vesiculosus. Marine Ecology Progress Series 544, 131–142.
Lack of fine-scale genetic structure and distant mating in natural populations of Fucus vesiculosus.Crossref | GoogleScholarGoogle Scholar |

Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
Micro-checker: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar |

Wallace, A. L., Klein, A. S., and Mathieson, A. C. (2004). Determining the affinities of salt marsh fucoids using microsatellite markers: evidence of hybridisation and introgression between two species of Fucus (Phaeophyta) in a Maine estuary. Journal of Phycology 40, 1013–1027.
Determining the affinities of salt marsh fucoids using microsatellite markers: evidence of hybridisation and introgression between two species of Fucus (Phaeophyta) in a Maine estuary.Crossref | GoogleScholarGoogle Scholar |

Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.

Wernberg, T., Coleman, M. A., Bennett, S., Thomsen, M. S., Tuya, F., and Kelaher, B. P. (2018). Genetic diversity and ecosystem vulnerability to climatic stress. Scientific Reports 8, 1851.
Genetic diversity and ecosystem vulnerability to climatic stress.Crossref | GoogleScholarGoogle Scholar |

Womersley, H. B. S. (1987). ‘The Marine Benthic Flora of Southern Australia. Part II.’ (South Australian Government Printer: Adelaide, SA, Australia.)