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RESEARCH ARTICLE

Re-assessing the origins of the invasive mussel Mytilus galloprovincialis in southern Africa

G. I. Zardi A , C. D. McQuaid A , R. Jacinto B , C. R. Lourenço A , E. A. Serrão B and K. R. Nicastro B C
+ Author Affiliations
- Author Affiliations

A Department of Zoology and Entomology, Rhodes University, Grahamstown, 6140, South Africa.

B CCMAR (Centro de Ciencias do Mar), CIMAR Laboratório Associado, Universidade do Algarve, Campus de Gambelas, PT-8005-139 Faro, Portugal.

C Corresponding author. Email: katynicastro@gmail.com

Marine and Freshwater Research 69(4) 607-613 https://doi.org/10.1071/MF17132
Submitted: 17 May 2017  Accepted: 16 October 2017   Published: 6 February 2018

Abstract

Retracing the origins of invasive species is a first critical step in identifying potential mechanisms of introduction, implementation of management strategies and forecasting the spread of the invader. Mytilus galloprovincialis is an intertidal mussel that is widely distributed in many temperate and subtropical regions. It is invasive worldwide and the most successful invasive marine species in southern Africa. Previous studies have examined genetic relationships between a few South African populations from the south-western coast and other worldwide populations, presenting evidence of a north-eastern Atlantic origin of the invasion. Here, a combination of nuclear (Me15/16 PCR-based) and mitochondrial (16S restriction fragment-length polymorphism; 16S RFLP) DNA assays was applied to infer the origin of this strong invader across its entire southern African distribution (South Africa and Namibia). The 16S RFLP confirmed the northern hemisphere as being the likely sole source of invasion. Additionally, the frequencies of haplotypes at the 16S marker and alleles at the Me15/16 locus point to north-eastern Atlantic shores as the most likely origin throughout the Namibian and South African distribution of the species.

Additional keywords: biogeography, intraspecific biodiversity, invasive species, mitochondrial DNA markers, nuclear DNA markers.


References

Assis, J., Zupan, M., Nicastro, K. R., Zardi, G. I., McQuaid, C. D., and Serrão, E. A. (2015). Oceanographic conditions limit the spread of a marine invader along southern African shores. PLoS One 10, e0128124.
Oceanographic conditions limit the spread of a marine invader along southern African shores.Crossref | GoogleScholarGoogle Scholar |

Bierne, N., Borsa, P., Daguin, C., Jollivet, D., Viard, F., Bonhomme, F., and David, P. (2003). Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis. Molecular Ecology 12, 447–461.
Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFahurY%3D&md5=68b3ffcfab1ecaaa24e89bde112088bfCAS |

Borsa, P., Daguin, C., Caetano, S. R., and Bonhomme, F. (1999). Nuclear-DNA evidence that northeastern Atlantic Mytilus trossulus mussels carry M. edulis genes. The Journal of Molluscan Studies 65, 504–507.
Nuclear-DNA evidence that northeastern Atlantic Mytilus trossulus mussels carry M. edulis genes.Crossref | GoogleScholarGoogle Scholar |

Bownes, S. J., and McQuaid, C. D. (2009). Mechanisms of habitat segregation between an invasive and an indigenous mussel: settlement, post-settlement mortality and recruitment. Marine Biology 156, 991–1006.
Mechanisms of habitat segregation between an invasive and an indigenous mussel: settlement, post-settlement mortality and recruitment.Crossref | GoogleScholarGoogle Scholar |

Branch, G. M., and Steffani, N. C. (2004). Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). Journal of Experimental Marine Biology and Ecology 300, 189–215.
Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck).Crossref | GoogleScholarGoogle Scholar |

Brown, M., and Hockey, P. A. R. (2007). The status and distribution of African black oystercatchers Haematopus moquini in KwaZulu–Natal, South Africa. Ostrich 78, 93–96.
The status and distribution of African black oystercatchers Haematopus moquini in KwaZulu–Natal, South Africa.Crossref | GoogleScholarGoogle Scholar |

Carlton, J. T., and Geller, J. B. (1993). Ecological roulette: the global transport of nonindigenous marine organisms. Science 261, 78–82.
Ecological roulette: the global transport of nonindigenous marine organisms.Crossref | GoogleScholarGoogle Scholar |

Coleman, R. A., and Hockey, P. A. R. (2008). Effects of an alien invertebrate species and wave action on prey selection by African black oystercatchers (Haematopus moquini). Austral Ecology 33, 232–240.
Effects of an alien invertebrate species and wave action on prey selection by African black oystercatchers (Haematopus moquini).Crossref | GoogleScholarGoogle Scholar |

Currat, M., Ruedi, M., Petit, R. J., and Excoffier, L. (2008). The hidden side of invasions: massive introgression by local genes. Evolution 62, 1908–1920.

Daguin, C., and Borsa, P. (2000). Genetic relationships of Mytilus galloprovincialis Lamarck populations worldwide: evidence from nuclear-DNA markers. Geological Society of London, Special Publications 177, 389–397.
Genetic relationships of Mytilus galloprovincialis Lamarck populations worldwide: evidence from nuclear-DNA markers.Crossref | GoogleScholarGoogle Scholar |

Darling, J. A., Bagley, M. J., Roman, J. O. E., Tepolt, C. K., and Geller, J. B. (2008). Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Molecular Ecology 17, 4992–5007.
Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXps1eqsQ%3D%3D&md5=638b543efbb91584af6deed6c675a891CAS |

Department of Agriculture, Forestry and Fisheries (2012). South Africa’s Aquaculture Yearbook 2012. (Department of Agriculture, Forestry and Fisheries: Cape Town, South Africa.) Available at http://www.nda.agric.za/doaDev/sideMenu/fisheries/03_areasofwork/Aquaculture/AquaDocumentation/Aquaculture%20Annual%20Reports/AQUACULTURE%20YEARBOOK%202012.pdf [Verified 1 February 2018].

Drake, J. M., and Lodge, D. M. (2004). Global hot spots of biological invasions: evaluating options for ballast-water management. Proceedings of the Royal Society of London. Series B, Biological Sciences 271, 575–580.
Global hot spots of biological invasions: evaluating options for ballast-water management.Crossref | GoogleScholarGoogle Scholar |

Drygala, F., Korablev, N., Ansorge, H., Fickel, J., Isomursu, M., Elmeros, M., Kowalczyk, R., Baltrunaite, L., Balciauskas, L., and Saarma, U. (2016). Homogenous population genetic structure of the non-native Raccoon dog (Nyctereutes procyonoides) in Europe as a result of rapid population expansion. PLoS One 11, e0153098.
Homogenous population genetic structure of the non-native Raccoon dog (Nyctereutes procyonoides) in Europe as a result of rapid population expansion.Crossref | GoogleScholarGoogle Scholar |

Estoup, A., and Guillemaud, T. (2010). Reconstructing routes of invasion using genetic data: why, how and so what? Molecular Ecology 19, 4113–4130.
Reconstructing routes of invasion using genetic data: why, how and so what?Crossref | GoogleScholarGoogle Scholar |

Gardner, J. P. A., and Westfall, K. M. (2012). Geographic distribution and molecular identification of a metapopulation of blue mussels (genus Mytilus) in northeastern New Zealand. The Journal of Molluscan Studies 78, 66–73.
Geographic distribution and molecular identification of a metapopulation of blue mussels (genus Mytilus) in northeastern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Geller, J. B., Darling, J. A., and Carlton, J. T. (2010). Genetic perspectives on marine biological invasions. Annual Review of Marine Science 2, 367–393.
Genetic perspectives on marine biological invasions.Crossref | GoogleScholarGoogle Scholar |

Gérard, K., Bierne, N., Borsa, P., Chenuil, A., and Féral, J. P. (2008). Pleistocene separation of mitochondrial lineages of Mytilus spp. mussels from northern and southern hemispheres and strong genetic differentiation among southern populations. Molecular Phylogenetics and Evolution 49, 84–91.
Pleistocene separation of mitochondrial lineages of Mytilus spp. mussels from northern and southern hemispheres and strong genetic differentiation among southern populations.Crossref | GoogleScholarGoogle Scholar |

Gosling, E. M. (1992). Systematics and geographic distribution of Mytilus. In ‘The Mussel Mytilus; Ecology, Physiology, Genetic and Culture. Developments in Aquaculture and Fisheries Science, Vol. 25’. (Ed. E. M. Gosling.) (Elsevier Science: Amsterdam, Netherlands.)

Gosling, E., Doherty, S., and Howley, N. (2008). Genetic characterization of hybrid mussel (Mytilus) populations on Irish coasts. Journal of the Marine Biological Association of the United Kingdom 88, 341–346.
Genetic characterization of hybrid mussel (Mytilus) populations on Irish coasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjs1akt7g%3D&md5=b6e055eb9a0db9ef9151e1f132227133CAS |

Gosset, C. C., and Bierne, N. (2013). Differential introgression from a sister species explains high FST outlier loci within a mussel species. Journal of Evolutionary Biology 26, 14–26.
Differential introgression from a sister species explains high FST outlier loci within a mussel species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s7nvFCrtw%3D%3D&md5=a754239b374f485206d45b5879ddaec5CAS |

Grant, W. S., and Cherry, M. I. (1985). Mytilus galloprovincialis Lmk. in southern Africa. Journal of Experimental Marine Biology and Ecology 90, 179–191.
Mytilus galloprovincialis Lmk. in southern Africa.Crossref | GoogleScholarGoogle Scholar |

Hamer, B., Korlevic, M., Durmisi, E., Nerlovic, V., and Bierne, N. (2012). Nuclear marker Me15–16 analyses of Mytilus galloprovincialis populations along the eastern Adriatic coast. Cahiers de Biologie Marine 53, 35–44.

Hilbish, T. J., Mullinax, A., Dolven, S. I., Meyer, A., Koehn, R. K., and Rawson, P. D. (2000). Origin of the antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration. Marine Biology 136, 69–77.
Origin of the antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration.Crossref | GoogleScholarGoogle Scholar |

Hilbish, T. J., Lima, F. P., Brannock, P. M., Fly, E. K., Rognstad, R. L., and Wethey, D. S. (2012). Change and stasis in marine hybrid zones in response to climate warming. Journal of Biogeography 39, 676–687.
Change and stasis in marine hybrid zones in response to climate warming.Crossref | GoogleScholarGoogle Scholar |

Hulme, P. E. (2009). Trade, transport and trouble: managing invasive species pathways in an era of globalization. Journal of Applied Ecology 46, 10–18.
Trade, transport and trouble: managing invasive species pathways in an era of globalization.Crossref | GoogleScholarGoogle Scholar |

Inoue, K., Waite, J. H., Matsuoka, M., Odo, S., and Harayama, S. (1995). Interspecific variations in adhesive protein sequences of Mytilus edulis, M. galloprovincialis, and M. trossulus. The Biological Bulletin 189, 370–375.
Interspecific variations in adhesive protein sequences of Mytilus edulis, M. galloprovincialis, and M. trossulus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK287gslSmtw%3D%3D&md5=dc632ed1f3582dd5aefef65e899ff15fCAS |

Kohler, S. A., Connan, M., Hill, J. M., Mablouké, C., Bonnevie, B., Ludynia, K., Kemper, J., Huisamen, J., Underhill, L. G., and Cherel, Y. (2011). Geographic variation in the trophic ecology of an avian rocky shore predator, the African black oystercatcher, along the southern African coastline. Marine Ecology Progress Series 435, 235–249.
Geographic variation in the trophic ecology of an avian rocky shore predator, the African black oystercatcher, along the southern African coastline.Crossref | GoogleScholarGoogle Scholar |

Lourenço, C. R., Nicastro, K. R., Serrão, E. A., Castilho, R., and Zardi, G. I. (2015). Behind the mask: cryptic genetic diversity of Mytilus galloprovincialis along southern European and northern African shores. The Journal of Molluscan Studies 81, 380–387.
Behind the mask: cryptic genetic diversity of Mytilus galloprovincialis along southern European and northern African shores.Crossref | GoogleScholarGoogle Scholar |

Luttikhuizen, P. C., Koolhaas, A., Bol, A., and Piersma, T. (2002). Mytilus galloprovincialis-type foot-protein-1 alleles occur at low frequency among mussels in the Dutch Wadden Sea. Journal of Sea Research 48, 241–245.
Mytilus galloprovincialis-type foot-protein-1 alleles occur at low frequency among mussels in the Dutch Wadden Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVKmtL8%3D&md5=7168270771fc4b7fb104060c8564e338CAS |

McDonald, J. H., Seed, R., and Koehn, R. K. (1991). Allozymes and morphometric characters of three species of Mytilus in the northern and southern hemispheres. Marine Biology 111, 323–333.
Allozymes and morphometric characters of three species of Mytilus in the northern and southern hemispheres.Crossref | GoogleScholarGoogle Scholar |

McQuaid, C. D., and Phillips, T. E. (2000). Limited wind-driven dispersal of intertidal mussel larvae: in situ evidence from the plankton and the spread of the invasive species Mytilus galloprovincialis in South Africa. Marine Ecology Progress Series 201, 211–220.
Limited wind-driven dispersal of intertidal mussel larvae: in situ evidence from the plankton and the spread of the invasive species Mytilus galloprovincialis in South Africa.Crossref | GoogleScholarGoogle Scholar |

McQuaid, C. D., Porri, F., Nicastro, K. R., and Zardi, G. I. (2015). Simple, scale-dependent patterns emerge from very complex effects: an example from the intertidal mussels Mytilus galloprovincialis and Perna perna. Oceanography and Marine Biology – an Annual Review 53, 127–156.
Simple, scale-dependent patterns emerge from very complex effects: an example from the intertidal mussels Mytilus galloprovincialis and Perna perna.Crossref | GoogleScholarGoogle Scholar |

Mead, A., Carlton, J. T., Griffiths, C. L., and Rius, M. (2011). Revealing the scale of marine bioinvasions in developing regions: a South African re-assessment. Biological Invasions 13, 1991–2008.
Revealing the scale of marine bioinvasions in developing regions: a South African re-assessment.Crossref | GoogleScholarGoogle Scholar |

Nicastro, K. R., Zardi, G. I., and McQuaid, C. D. (2008). Movement behaviour and mortality in invasive and indigenous mussels: resilience and resistance strategies at different spatial scales. Marine Ecology Progress Series 372, 119–126.
Movement behaviour and mortality in invasive and indigenous mussels: resilience and resistance strategies at different spatial scales.Crossref | GoogleScholarGoogle Scholar |

Nicastro, K. R., Zardi, G. I., and McQuaid, C. D. (2010). Differential reproductive investment, attachment strength and mortality of invasive and indigenous mussels across heterogeneous environments. Biological Invasions 12, 2165–2177.
Differential reproductive investment, attachment strength and mortality of invasive and indigenous mussels across heterogeneous environments.Crossref | GoogleScholarGoogle Scholar |

Palumbi, S. R. (1996). Nucleic acids II: the polymerase chain reaction. Molecular Systematics 2, 205–247.

Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=628cd04355508114bafe3d36e17c81b4CAS |

Robinson, T. B., Branch, G. M., Griffiths, C. L., Govender, A., and Hockey, P. A. (2007). Changes in South African rocky intertidal invertebrate community structure associated with the invasion of the mussel Mytilus galloprovincialis. Marine Ecology Progress Series 340, 163–171.
Changes in South African rocky intertidal invertebrate community structure associated with the invasion of the mussel Mytilus galloprovincialis.Crossref | GoogleScholarGoogle Scholar |

Roman, J., and Darling, J. A. (2007). Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology & Evolution 22, 454–464.
Paradox lost: genetic diversity and the success of aquatic invasions.Crossref | GoogleScholarGoogle Scholar |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |

Saarman, N. P., and Pogson, G. H. (2015). Introgression between invasive and native blue mussels (genus Mytilus) in the central California hybrid zone. Molecular Ecology 24, 4723–4738.
Introgression between invasive and native blue mussels (genus Mytilus) in the central California hybrid zone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFGitL3J&md5=748c055b7d1c6130d63bc666859c52e8CAS |

Sambrook, J., Fritseh, E. F., and Maniatis, T. (1989). ‘Molecular coning. A Laboratory Manual’, 2nd edn. (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA.)

Sanjuan, A., Zapata, C., and Alvarez, G. (1994). Mytilus galloprovincialis and M. edulis on the coasts of the Iberian Peninsula. Marine Ecology Progress Series 113, 131–146.
Mytilus galloprovincialis and M. edulis on the coasts of the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |

Sanjuan, A., Zapata, C., and Alvarez, G. (1997). Genetic differentiation in Mytilus galloprovincialis Lmk. throughout the world. Ophelia 47, 13–31.
Genetic differentiation in Mytilus galloprovincialis Lmk. throughout the world.Crossref | GoogleScholarGoogle Scholar |

Śmietanka, B., Zbawicka, M., Wołowicz, M., and Wenne, R. (2004). Mitochondrial DNA lineages in the European populations of mussels (Mytilus spp.). Marine Biology 146, 79–92.
Mitochondrial DNA lineages in the European populations of mussels (Mytilus spp.).Crossref | GoogleScholarGoogle Scholar |

Steffani, C. N., and Branch, G. M. (2003). Spatial comparisons of populations of an indigenous limpet Scutellastra argenvillei and an alien mussel Mytilus galloprovincialis along a gradient of wave energy. African Journal of Marine Science 25, 195–212.
Spatial comparisons of populations of an indigenous limpet Scutellastra argenvillei and an alien mussel Mytilus galloprovincialis along a gradient of wave energy.Crossref | GoogleScholarGoogle Scholar |

Steffani, C. N., and Branch, G. M. (2005). Mechanisms and consequences of competition between an alien mussel, Mytilus galloprovincialis, and an indigenous limpet, Scutellastra argenvillei. Journal of Experimental Marine Biology and Ecology 317, 127–142.
Mechanisms and consequences of competition between an alien mussel, Mytilus galloprovincialis, and an indigenous limpet, Scutellastra argenvillei.Crossref | GoogleScholarGoogle Scholar |

Vera, M., Díez del Molino, D., and García Marín, J. L. (2016). Genomic survey provides insights into the evolutionary changes that occurred during European expansion of the invasive mosquitofish (Gambusia holbrooki). Molecular Ecology 25, 1089–1105.
Genomic survey provides insights into the evolutionary changes that occurred during European expansion of the invasive mosquitofish (Gambusia holbrooki).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xjs1Cgsbc%3D&md5=adbfdb39e2529e2e2deb2027ab250ecfCAS |

Vernon, C. (2004). Status and abundance of the African black oystercatcher Haematopus moquini at the eastern limit of its breeding range. Ostrich 75, 243–249.
Status and abundance of the African black oystercatcher Haematopus moquini at the eastern limit of its breeding range.Crossref | GoogleScholarGoogle Scholar |

Voisin, M., Engel, C. R., and Viard, F. (2005). Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proceedings of the National Academy of Sciences of the United States of America 102, 5432–5437.
Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslaqsb8%3D&md5=d0459fbeb145239cd53e586c5b3a10a3CAS |

Waite, J. H. (1992) The formation of Mussel byssus: anatomy of a natural manufacturing process. In ‘Structure, Cellular Synthesis and Assembly of Biopolymers. Results and Problems in Cell Differentiation. Topical Volumes in Developmental Biology, Vol. 19. (Ed. S. T. Case.) pp. 27–54. (Springer: Berlin, Germany.)

Westfall, K. M., and Gardner, J. P. A. (2010). Genetic diversity of southern hemisphere blue mussels (Bivalvia: Mytilidae) and the identification of non-indigenous taxa. Biological Journal of the Linnean Society. Linnean Society of London 101, 898–909.
Genetic diversity of southern hemisphere blue mussels (Bivalvia: Mytilidae) and the identification of non-indigenous taxa.Crossref | GoogleScholarGoogle Scholar |

Westfall, K., and Gardner, J. A. (2013). Interlineage Mytilus galloprovincialis Lmk. 1819 hybridization yields inconsistent genetic outcomes in the southern hemisphere. Biological Invasions 15, 1493–1506.
Interlineage Mytilus galloprovincialis Lmk. 1819 hybridization yields inconsistent genetic outcomes in the southern hemisphere.Crossref | GoogleScholarGoogle Scholar |

Westfall, K. M., Wimberger, P. H., and Gardner, J. P. A. (2010). An RFLP assay to determine if Mytilus galloprovincialis Lmk. (Mytilidae; Bivalvia) is of northern or southern hemisphere origin. Molecular Ecology Resources 10, 573–575.
An RFLP assay to determine if Mytilus galloprovincialis Lmk. (Mytilidae; Bivalvia) is of northern or southern hemisphere origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXms1amurY%3D&md5=32692479133e4708265aa0674dd76307CAS |

Zardi, G., McQuaid, C., Teske, P., and Barker, N. (2007). Unexpected genetic structure of mussel populations in South Africa: indigenous Perna perna and invasive Mytilus galloprovincialis. Marine Ecology Progress Series 337, 135–144.
Unexpected genetic structure of mussel populations in South Africa: indigenous Perna perna and invasive Mytilus galloprovincialis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXovFWmtbw%3D&md5=871266a73e5d349a44078bbfd934ca4cCAS |