Abstract
The species is often described as the basic unit of biology, yet defining what constitutes a species has been a long-standing challenge. The advent of modern molecular techniques in conjunction with advanced analytical approaches now provide new opportunities for the robust and repeatable delineation of taxa from previously difficult to assess species complexes. Using marine mussels of the genus Mytilus (smooth-shelled blue mussels of the globally distributed Mytilus edulis species complex) we tested regionally differentiated putative taxa from the Northern and Southern hemispheres using a Bayesian species delimitation model that infers species trees. Using a multilocus panel of 54 single nucleotide polymorphic loci (SNPs) we tested four alternative hypotheses against the hypothesis of the currently recognised taxonomy to better understand the evolutionary history and the contemporary species of this complex. Only one model provided a better fit than the contemporary taxonomy model: this best fit model included the three reference Northern hemisphere taxa (M. edulis, M. galloprovincialis, M. trossulus) plus M. chilensis (Chile), M. platensis (Argentina), M. planulatus (Australia) and the newly recognised M. aoteanus (New Zealand). Phylogenetic reconstruction based on our nuclear DNA-based SNP data suggests that M. trossulus is the oldest of the modern smooth-shelled blue mussels, that a first migration event from the north to the south occurred that gave rise to M. platensis and M. chilensis in South America, subsequently that M. edulis and M. galloprovincialis diverged in the Northern hemisphere, and that subsequently again there was a second migration event from the north that gave rise to M. planulatus in Australia and M. aoteanus in New Zealand. Our findings provide very strong support for earlier mitochondrial DNA-based phylogenetic findings for globally distributed blue mussels and also help to clarify uncertainty about the number of north-to-south migration events that gave rise to important Mytilus speciation events in South America and in Australasia.
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Genetic homogeneity and weak signatures of local adaptation in the marine mussel Mytilus chilensis
Shedding light on variation in reproductive success through studies of population genetic structure in a Southeast Pacific Coast mussel
Boundaries and hybridization in a secondary contact zone between freshwater mussel species (Family:Unionidae)
Data availability
All data analysed during this study are included in this published article. Additionally, the DNA sequences are stored in GenBank (KT713378–82; HQ257471; KJ871039–57; KT713368–74).
References
Sites, J. W. & Marshall, J. C. Delimiting species: A renaissance issue in systematic biology. Trends Ecol. Evol. 18 (9), 462–470 (2003).
Camargo, A. & Sites, J. W. Species delimitation: A decade after the renaissance. In The Species Problem –Ongoing Issues, (ed Pavlinov, I. Y.) Rijeka: InTech, 225–247 (2013).
Yang, Z. & Rannala, B. Unguided species delimitation using DNA sequence data from multiple loci. Mol. Biol. Evol. 31 (12), 3125–3135 (2014).
Gardner, J. P. A., Oyarzún, P. A., Toro, J. E., Wenne, R. & Zbawicka, M. Phylogeography of Southern hemisphere blue mussels of the genus Mytilus: evolution, biosecurity, aquaculture and food labelling. Oceanogr. Mar. Biol. Annu. Rev. 59, 139–232 (2021).
Oyarzún, P. A., Toro, J. E., Nuñez, J. J., Suarez-Villota, E. & Gardner, J. P. A. Blue mussels of the Mytilus Edulis species complex from South america: the application of species delimitation models to DNA sequence variation. PLoS ONE. 16 (9). https://doi.org/10.1371/journal.pone.0256961 (2021). e0256961.
Koehn, R. K., Hall, J. G., Innes, D. J. & Zera, A. J. Genetic differentiation of Mytilus Edulis in Eastern North America. Mar. Biol. 79, 117–126 (1984).
McDonald, J. H., Seed, R. & Koehn, R. K. Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern hemispheres. Mar. Biol. 111, 323–333 (1991).
Gosling, E. M. Systematics and geographic distribution of Mytilus. In The Mussel Mytilus: Ecology, Physiology, Genetics and Culture; (ed Gosling, E. M.) Elsevier: Amsterdam, The Netherlands, 1–20 (1992).
Hilbish, T. J. et al. Origin of the Antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration. Mar. Biol. 136, 69–77 (2000).
Crooks, J. A. Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97, 153–151 (2002).
Borthagaray, A. I. & Carranza, A. Mussels as ecosystem engineers: their contribution to species richness in a Rocky Littoral community. Acta Oecol. 31, 243–250 (2007).
FAO. The State of World Fisheries and Aquaculture 2024 – Blue Transformation in action. Rome. (2024).
Michalek, K., Ventura, A. & Sanders, T. Mytilus hybridisation and impact on aquaculture: A minireview. Mar. Genomics. 27, 3–7 (2016).
González-Poblete, E., Hurtado, F. C., Rojo, C. & Norambuena, R. Blue mussel aquaculture in chile: small or large scale industry? Aquaculture 493, 113–122 (2018).
Larraín, M. A., Zbawicka, M., Araneda, C., Gardner, J. P. A. & Wenne, R. Native and invasive taxa on the Pacific Coast of South america: impacts on aquaculture, traceability and biodiversity of blue mussels (Mytilus spp). Evol. Appl. 11, 298–311 (2018).
Oyarzún, P. A., Toro, J. E., Cañete, J. I. & Gardner, J. P. A. Bioinvasion threatens the genetic integrity of native diversity and a natural hybrid zone: smooth-shelled blue mussels (Mytilus spp.) in the Strait of Magellan. Biol. J. Linn. Soc. 117, 574–585 (2016).
Zbawicka, M., Trucco, M. I. & Wenne, R. Single nucleotide polymorphisms in native South American Atlantic Coast populations of smooth shelled mussels: hybridization with invasive European Mytilus galloprovincialis. Genet. Sel. Evol. 50, 5 (2018).
Dias, P. J., Fotedar, S. & Snow, M. Characterisation of mussel (Mytilus sp.) populations in Western Australia and evaluation of potential genetic impacts of mussel Spat translocation from interstate. Mar. Freshw. Res. 65, 486–496 (2014).
Ab Rahim, E. S. et al. Species composition and hybridisation of mussel species (Bivalvia: Mytilidae) in Australia. Mar. Freshw. Res. 67, 1955–1963 (2016).
Zbawicka, M., Wenne, R., Dias, P. J. & Gardner, J. P. A. Combined threats to native smooth-shelled mussels (genus Mytilus) in australia: bioinvasions and hybridisation. Zoo J. Linn. Soc. 194, 1194–1211 (2022).
Gardner, J. P. A., Wenne, R., Westfall, K. R. & Zbawicka, M. Invasive mussels threaten regional scale genetic diversity in Mainland and remote offshore locations: the need for baseline data and enhanced protection in the Southern ocean. Glob Change Biol. 22, 3182–3195 (2016).
Zbawicka, M., Gardner, J. P. A. & Wenne, R. Cryptic diversity in smooth-shelled mussels on Southern ocean islands: Connectivity, hybridisation and a marine invasion. Front. Zool. 16, 32 (2019).
Fraïsse, C. et al. Fine-grained habitat associated genetic connectivity in an admixed population of mussels in the small isolated kerguelen Islands. Peer Community J. 1, e10 (2021).
Westfall, K. M. & Gardner, J. P. A. Genetic diversity of Southern hemisphere blue mussels of the genus Mytilus (Mytilidae; Bivalvia) and the identification of non-indigenous taxa. Biol. J. Linn. Soc. 101, 898–909 (2010).
Westfall, K. M. & Gardner, J. P. A. Interlineage Mytilus galloprovincialis Lmk. 1819 hybridisation yields inconsistent genetic outcomes in three Southern hemisphere regions. Biol. Invasions. 15, 1493–1506 (2013).
Popovic, I., Matias, A. M. A., Bierne, N. & Riginos, C. Twin introductions by independent invader mussel lineages are both associated with recent admixture with a native congener in Australia. Evol. Appl. 13, 515–532 (2020).
Shaffer, H. & Thomson, R. Delimiting species in recent radiations. Syst. Biol. 6 (56), 896–906 (2007).
Shin, J., Kwon, S., Lee, J., Min, H. & Kim, N. Genetic diversity of maize kernel starch-synthesis genes with snaps. Genome 10 (49), 1287–1296 (2006).
Wenne, R. Single nucleotide polymorphism markers with applications in conservation and exploitation of aquatic natural populations. Animals 13 (6), 1089 (2023).
Gabur, I. et al. Finding invisible quantitative trait loci with missing data. Plant. Biotechnol. J. 12 (16), 2102–2112 (2018).
Meudt, H., Lockhart, P. & Bryant, D. Species delimitation and phylogeny of a new Zealand plant species radiation. BMC Ecol. Evol. 1 (9), 111 (2009).
Wanghe, C. et al. Phylogenetic relationship and taxonomic status of Gymnocypris eckloni (Schizothoracinae) based on specific locus amplified fragments sequencing. Front. Ecol. Evol. 10, 933632 (2022).
Kelly, J. & Thacker, R. New shallow water species of Caribbean Ircinia Nardo, 1833 (Porifera: Irciniidae). Zootaxa 4 (5072), 301–323 (2021).
Campbell, E., Gage, E., Gage, R. & Sperling, F. Single nucleotide polymorphism-based species phylogeny of greater fritillary butterflies (Lepidoptera: nymphalidae: Speyeria) demonstrates widespread mitonuclear discordance. Syst. Entomol. 2 (45), 269–280 (2019).
Martínez-Borrego, D., Arellano, E., González-Cózatl, F. & Rogers, D. Species delimitation and integrative taxonomy of the Reithrodontomys Mexicanus (Rodentia: Cricetidae) cryptic complex. Ecol. Evol. 13(8), e10355 (2023).
Yuan, Z. et al. Historical mitochondrial genome introgression confounds species delimitation: evidence from phylogenetic inference in the Odorrana Grahami species complex. Curr. Zool. 1 (69), 82–90 (2023).
Fujita, M. K., Leaché, A. D., Burbrink, F. T., McGuire, J. A. & Moritz, C. Coalescent-based species delimitation in an integrative taxonomy. Trends Ecol. Evol. 27 (9), 480–488 (2012).
Mason, N. A., Fletcher, N. K., Gill, B. A., Funk, W. C. & Zamudio, K. R. Coalescent-based species delimitation is sensitive to geographic sampling and isolation by distance. Syst. Biodiv. 18 (3), 269–280 (2020).
Kornai, D., Jiao, X., Ji, J., Flouri, T. & Yang, Z. Hierarchical heuristic species delimitation under the multispecies coalescent model with migration. Syst. Biol. 73 (6), 1015–1037 (2024).
Bryant, D., Bouckaert, R., Felsenstein, J., Rosenberg, N. A. & RoyChoudhury, A. Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis. Mol. Biol. Evol. 29, 1917–1932 (2012).
Leaché, A. D., Fujita, M. K., Minin, V. N. & Bouckaert, R. R. Species delimitation using Genome-Wide SNP data. Syst. Biol. 63 (4), 534–542 (2014).
Leaché, A. D. & Fujita, M. K. Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proc. R Soc. B Biol. Sci. 277, 3071–3077 (2010).
South, A. & rworldxtra Country boundaries at high resolution. R package version 1.01. (2023). https://CRAN.R-project.org/package=rworldxtra
Gabriel, S., Ziaugra, L. & Tabbaa, D. SNP genotyping using the sequenom massarray iPLEX platform. Curr Protoc. Hum. Genet Chapter 2: (2009). Unit 2.12.
Wenne, R., Bach, L., Zbawicka, M., Strand, J. & McDonald, J. H. A first report on coexistence and hybridization of Mytilus trossulus and M. edulis mussels in Greenland. Polar Biol. 39 (2), 343–355 (2016).
Zbawicka, M. et al. Genetic differentiation in Mytilus populations across climatic zones in Greenland. J Biogeogr. e70067 (2025).
Bouckaert, R. et al. BEAST 2: A software platform for bayesian evolutionary analysis. PLoS Comput. Biol. 10 (4), e1003537 (2014).
Kass, R. E. & Raftery, A. E. Bayes factors. J. Am. Stat. Assoc. 90, 773–795 (1995).
Matschiner, M. Species tree inference with SNP data. In: (eds Pereira-Santana, A., Gamboa-Tuz, S. D. & Rodríguez-Zapata, L. C.) Plant Comparative Genomics. Methods in Molecular Biology, vol 2512. Humana, New York (2022).
Riginos, C. & Cunningham, C. W. Local adaptation and species segregation in two mussel (Mytilus Edulis × Mytilus trossulus) hybrid zones. Mol. Ecol. 14, 381–400 (2005).
Rambaut, A. & FigTree (Version 1.4.2) [Software]. Institute of Evolutionary Biology, University of Edinburgh. (2018). Retrieved from http://tree.bio.ed.ac.uk/software/figtree/
Koehn, R. K. The genetics and taxonomy of species in the genus Mytilus. Aquaculture 94 (2–3), 125–145 (1991).
Gardner, J. P. A. Mytilus galloprovincialis (Lmk) (Bivalvia, Mollusca): the taxonomic status of the mediterranean mussel. Ophelia 35 (3), 219–243 (1992).
Seed, R. Systematics, evolution and distribution of mussels belonging to the genus Mytilus: an over-view. Am. Malacol Bull. 9, 123–137 (1992).
Illesca, A., Oyarzún, P. A., Toro, J. E. & Gardner, J. P. A. Morphometric variability of smooth-shelled blue mussels from the Pacific Coast of South America. Biol. J. Linn. Soc. 125, 194–209 (2018).
Powell, A. W. B. New Zealand molluscan systematics with descriptions of new species, part 3. Records Auckl. Inst. Museum. 5, 87–91 (1958).
Fleming, C. A. Notes on new Zealand recent and tertiary mussels (Mytilidae). Trans. R Soc. N Z. 87, 165–178 (1959).
Soot-Ryen, T. A report of the family mytilidae (Pelecypoda). Allan Hancock Pacifc Expedition. 20, 1–75 (1955).
Ravalo, L. G. O. Native and invasive smooth shelled blue mussels Mytilus spp in New Zealand: Evolutionary Biosecurity and Aquaculture Implications. PhD tesis, Victoria University of Wellington, New Zealand Available at – (2024). https://openaccess.wgtn.ac.nz/articles/thesis/Native_and_Invasive_Smooth_Shelled_Blue_Mussels_Mytilus_spp_in_New_Zealand_Evolutionary_Biosecurity_and_Aquaculture_Implications/25989046
Gérard, K., Bierne, N., Borsa, P., Chenuil, A. & Feral, J. P. Pleistocene separation of mitochondrial lineages of Mytilus spp. Mussels from Northern and Southern hemispheres and strong genetic differentiation among Southern populations. Mol. Phylogenet Evol. 49, 84–91 (2008).
Kiel, S. & Nielsen, S. N. Quaternary origin of the inverse latitudinal diversity gradient among Southern Chilean mollusks. Geology 38, 955–958 (2010).
Acknowledgements
We thank the CIPRES Science Gateway for providing access to its platform, which facilitated several of our analyses.
Funding
This work was funded by the projects FONDECYT 1230212 (JT) and FONDECYT 1251077 (POC).
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P.A.O.: Conceptualisation, methodology, and writing—review and editing. J.E.T.: Investigation and validation. M.Z.: Investigation and validation. R.W.: Investigation and validation. J.P.A.G.: Conceptualisation, and writing—review and editing. All authors have read and agreed to the published version of the manuscript.
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Oyarzún, P.A., Toro, J.E., Zbawicka, M. et al. Global species delimitation of smooth-shelled blue mussels in the Mytilus edulis complex.
Sci Rep (2025). https://doi.org/10.1038/s41598-025-29759-9
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DOI: https://doi.org/10.1038/s41598-025-29759-9
Keywords
- Cryptic species
- Molluscs
- SNPs
- Speciation
- Taxonomy
Source: Ecology - nature.com
