Limited population genetic variation but pronounced seascape genetic structuring in populations of the Mediterranean mussel (Mytilus galloprovincialis) from the eastern Adriatic Sea
Joanna S. Hamilton,
Marina Piria,
Ana Gavrilović,
Mirna Mrkonjić Fuka,
Lidija Svečnjak,
Slađana Nikolić,
Rigers Bakiu,
Jonathan P. A. Gardner,
Corresponding Author
Joanna S. Hamilton
School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand
Correspondence
Joanna S. Hamilton, School of Biological Sciences, Victoria University of Wellington, Wellington 6140, New Zealand.
Email: [email protected]
Contribution: Conceptualization (equal), Data curation (lead), Formal analysis (equal), Funding acquisition (equal), Investigation (equal), Methodology (equal), Resources (supporting), Software (equal), Validation (equal), Visualization (equal), Writing - original draft (equal), Writing - review & editing (lead)
Search for more papers by this authorMarina Piria
Department of Fisheries, Apiculture, Faculty of Agriculture, Wildlife Management and Special Zoology, University of Zagreb, Zagreb, Croatia
Department of Ecology and Vertebrate Zoology, Faculty of Biology and Environmental Protection, University of Łódź, Łódź, Poland
Contribution: Conceptualization (equal), Funding acquisition (equal), Methodology (equal), Project administration (supporting), Resources (lead), Writing - review & editing (supporting)
Search for more papers by this authorAna Gavrilović
Department of Fisheries, Apiculture, Faculty of Agriculture, Wildlife Management and Special Zoology, University of Zagreb, Zagreb, Croatia
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorMirna Mrkonjić Fuka
Department of Microbiology, Faculty of Agriculture, University of Zagreb, Zagreb, Croatia
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorLidija Svečnjak
Department of Fisheries, Apiculture, Faculty of Agriculture, Wildlife Management and Special Zoology, University of Zagreb, Zagreb, Croatia
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorSlađana Nikolić
Institute of Marine Biology, University of Montenegro, Kotor, Montenegro
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorRigers Bakiu
Department of Aquaculture and Fisheries, Faculty of Agriculture and Environment, Agricultural University of Tirana, Tirana, Albania
Albanian Center for Environmental Protection and Sustainable Development, Tirana, Albania
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorJonathan P. A. Gardner
School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand
Contribution: Conceptualization (equal), Formal analysis (equal), Funding acquisition (equal), Investigation (equal), Methodology (equal), Project administration (lead), Resources (lead), Software (equal), Supervision (lead), Validation (equal), Visualization (equal), Writing - original draft (equal), Writing - review & editing (lead)
Search for more papers by this authorJoanna S. Hamilton,
Marina Piria,
Ana Gavrilović,
Mirna Mrkonjić Fuka,
Lidija Svečnjak,
Slađana Nikolić,
Rigers Bakiu,
Jonathan P. A. Gardner,
Corresponding Author
Joanna S. Hamilton
School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand
Correspondence
Joanna S. Hamilton, School of Biological Sciences, Victoria University of Wellington, Wellington 6140, New Zealand.
Email: [email protected]
Contribution: Conceptualization (equal), Data curation (lead), Formal analysis (equal), Funding acquisition (equal), Investigation (equal), Methodology (equal), Resources (supporting), Software (equal), Validation (equal), Visualization (equal), Writing - original draft (equal), Writing - review & editing (lead)
Search for more papers by this authorMarina Piria
Department of Fisheries, Apiculture, Faculty of Agriculture, Wildlife Management and Special Zoology, University of Zagreb, Zagreb, Croatia
Department of Ecology and Vertebrate Zoology, Faculty of Biology and Environmental Protection, University of Łódź, Łódź, Poland
Contribution: Conceptualization (equal), Funding acquisition (equal), Methodology (equal), Project administration (supporting), Resources (lead), Writing - review & editing (supporting)
Search for more papers by this authorAna Gavrilović
Department of Fisheries, Apiculture, Faculty of Agriculture, Wildlife Management and Special Zoology, University of Zagreb, Zagreb, Croatia
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorMirna Mrkonjić Fuka
Department of Microbiology, Faculty of Agriculture, University of Zagreb, Zagreb, Croatia
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorLidija Svečnjak
Department of Fisheries, Apiculture, Faculty of Agriculture, Wildlife Management and Special Zoology, University of Zagreb, Zagreb, Croatia
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorSlađana Nikolić
Institute of Marine Biology, University of Montenegro, Kotor, Montenegro
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorRigers Bakiu
Department of Aquaculture and Fisheries, Faculty of Agriculture and Environment, Agricultural University of Tirana, Tirana, Albania
Albanian Center for Environmental Protection and Sustainable Development, Tirana, Albania
Contribution: Resources (supporting), Writing - review & editing (supporting)
Search for more papers by this authorJonathan P. A. Gardner
School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand
Contribution: Conceptualization (equal), Formal analysis (equal), Funding acquisition (equal), Investigation (equal), Methodology (equal), Project administration (lead), Resources (lead), Software (equal), Supervision (lead), Validation (equal), Visualization (equal), Writing - original draft (equal), Writing - review & editing (lead)
Search for more papers by this authorAbstract
Population genetic analysis of variation at five neutral microsatellite loci for Mediterranean mussels (Mytilus galloprovincialis) from 18 sites along the eastern Adriatic Sea revealed little or no spatial variation. In contrast, seascape genetics analysis revealed a pronounced locus-specific gradient in allelic and genotypic frequencies across the study region. At a sixth locus, MGE7, the frequencies of two alleles, MGE7243 and MGE7249, were strongly associated, negatively and positively, respectively, with a single environmental variable – minimum salinity (minSAL). The frequency of the MGE7243/243 homozygous genotype was strongly negatively associated with minSAL, whereas the frequencies of the MGE7246/249 and the MGE7249/249 genotypes were strongly positively correlated with minSAL. Interpretation of these pronounced gradients is confounded by the fact that minSAL and another environmental variable, maximum sea surface temperature (maxSST), are highly correlated (R = −.911) and are therefore not necessarily acting independently. BLAST searches of the MGE7 locus against M. galloprovincialis whole genome shotgun sequence returned an alignment with contig mg10_S01094 (accession UYJE01010330.1) and 7 predicted M. galloprovincialis proteins VDI82194.1 - VDI82200.1. Conserved domain searches revealed a similar structure to the transcriptional regulator Msx2-interacting protein. The BLASTp search also returned significant alignments to Msx2-interacting proteins in Mytilus coruscus, Crassostrea virginica, and Haliotis rubra. The existence of the MGE7 gradient highlights the role that environmental variation may play in retarding gene flow among wild M. galloprovincialis populations, and also how the success of collection of young mussels (spat) from one site and their transfer to another site (the farm) may be influenced by a single factor such as minSAL or maxSST on a localized scale.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are openly available in Dryad at [https://doi.org/10.5061/dryad.p8cz8w9t8].
Supporting Information
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Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Anderson, M. J., Gorley, R. N., & Clarke, K. R. (2008). Permanova+ for PRIMER: Guide to software and statistical methods. PRIMER-e.
- Araneda, C., Noriega, X., Jilberto, F., Ruíz, J., Jara, C., Lafarga, F., & Larraín, M. A. (2016). Development of genome-wide microsatellite resources in a commercially important mussel species (Mytilus chilensis). Animal Genetics, 47(3), 387–388. https://doi.org/10.1111/age.12398
- Arieti, F., Gabus, C., Tambalo, M., Huet, T., Round, A., & Thore, S. (2014). The crystal structure of the Split end protein SHARP adds a new layer of complexity to proteins containing RNA recognition motifs. Nucleic Acids Research, 42(10), 6742–6752. https://doi.org/10.1093/nar/gku277
- Arribas, L. P., Donnarumma, L., Paloma, M. G., & Scrosati, R. A. (2014). Intertidal mussels as ecosystem engineers: Their associated invertebrate biodiversity under contrasting wave exposures. Marine Biodiversity, 44, 203–211. https://doi.org/10.1007/s12526-014-0201-z
- Artegiani, A., Bregant, D., Paschini, E., Pinardi, N., Raicich, F., & Russo, A. (1997). The Adriatic Sea general circulation. Part I: Air-Sea interactions and water mass structure. Journal of Physical Oceanography, 27, 1492–1514. https://doi.org/10.1175/1520-0485(1997)027<1492:TASGCP>2.0.CO;2
- Bellafiore, D., Guarnieri, A., Grilli, F., Penna, P., Bortoluzzi, G., Giglio, F., & Pinardi, N. (2011). Study of the hydrodynamical processes in the Boka Kotorska Bay with a finite element model. Dynamics of Atmospheres and Oceans, 52, 298–321. https://doi.org/10.1016/j.dynatmoce.2011.03.005
- Böhm, E., Banzon, V., D'Acunzo, E., D'Ortenzo, F., & Santoleri, R. (2003). Adriatic Sea surface temperature and ocean colour variability during the MFSPP. Annales Geophysicae, 21, 137–149. https://doi.org/10.5194/angeo-21-137-2003
- Bonacci, O., Željković, I., & Galić, A. (2013). Karst rivers' particularity: An example from Dinaric karst (Croatia/Bosnia and Herzegovina). Environmental Earth Sciences, 70(2), 963–974. https://doi.org/10.1007/s12665-012-2187-9
- Braby, C. E., & Somero, G. N. (2006). Following the heart: Temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). Journal of Experimental Biology, 209, 2554–2566. https://doi.org/10.1242/jeb.02259
- Branch, G. M., & Steffani, C. N. (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. https://doi.org/10.1016/j.jembe.2003.12.007
- Bray, L., Kassis, D., & Hall-Spencer, J. M. (2017). Assessing larval connectivity for marine spatial planning in the Atlantic. Marine Environmental Research, 125, 73–81. https://doi.org/10.1016/j.marenvres.2017.01.006
- Cárcamo, D. (2021). Does marine geospatial/environmental variation affect genetic variation? A meta-analysis. MSc Thesis. Victoria University of Wellington. https://openaccess.wgtn.ac.nz/articles/thesis/Does_marine_geospatial_environmental_variation_affect_genetic_variation_A_meta-analysis/16573280/1
- Da Ros, L., Bressan, M., & Marin, M. G. (1985). Reproductive cycle of the mussel (Mytilus galloprovincialis Lmk) in Venice lagoon (North Adriatic). Italian Journal of Zoology, 52(3–4), 223–229. https://doi.org/10.1080/11250008509440522
10.1080/11250008509440522 Google Scholar
- Daniels, E. Q., & Litvaitis, M. K. (2017). Does peripheral dislodgement contribute to heterozygote deficiencies in blue mussels? Invertebrate Biology, 136(3), 301–308. https://doi.org/10.1111/ivb.12183
- Di Camillo, C. G., & Cerrano, C. (2015). Mass mortality events in the NW Adriatic Sea: Phase shift from slow- to fast- growing organisms. PLoS One, 10(5), e0126689. https://doi.org/10.1371/journal.pone.0126689
- Diz, A. P., & Presa, P. (2008). Regional patterns of microsatellite variation in Mytilus galloprovincialis from the Iberian Peninsula. Marine Biology, 154, 227–286. https://doi.org/10.1007/s00227-008-0921-3
- Diz, A. P., & Presa, P. (2009). The genetic diversity pattern of Mytilus galloprovincialis in Galician Rías (NW Iberian estuaries). Aquaculture, 287, 278–285. https://doi.org/10.1016/j.aquaculture.2008.10.029
- Do, C., Waples, R. S., Peel, D., Macbeth, G. M., Tillett, B. J., & Ovenden, J. R. (2014). NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources, 14(1), 209–214. https://doi.org/10.1111/1755-0998.12157
- Dubois, M., Rossi, V., Ser-Giacomi, E., Arnaud-Haond, S., López, C., & Hernández-García, E. (2016). Linking basin-scale connectivity, oceanography and population dynamics for the conservation and management of marine ecosystems. Global Ecology and Biogeography, 25, 503–515. https://doi.org/10.1111/geb.12431
- Đurović, B., Đurović, I., Joksimović, A., Crnojević, V., Đukanović, S., & Pestorić, B. (2018). Monitoring the eutrophication using Landsat 8 in the Boka Kotorska Bay. Acta Adriatica, 59(1), 17–34. https://doi.org/10.32582/aa.59.1.2
- Earl, D. A., & von Holdt, B. M. (2012). Structure harvester: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetic Resources, 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7
- Estournel, C., Marsaleix, P., & Ulses, C. (2021). A new assessment of the circulation of Atlantic and intermediate waters in the eastern Mediterranean. Progress in Oceanography, 198, 102673. https://doi.org/10.1016/j.pocean.2021.102673
- Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
- Evans, T. G., & Somero, G. N. (2010). Phosphorylation events catalyzed by major cell Signalling proteins differ in response to thermal and osmotic stress among native (Mytilus californianus and Mytilus trossulus) and invasive (Mytilus galloprovincialis) species of mussels. Physiological and Biochemical Zoology, 83(6), 984–996. https://doi.org/10.1086/656192
- Excoffier, L., & Lischer, H. E. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetic analyses under Linux and windows. Molecular Ecology Resources, 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
- Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics, 131, 479–491. https://doi.org/10.1093/genetics/131.2.479
- Fischer, M. C., Rellstab, C., Leuzinger, M., Roumet, M., Gugerli, F., Shimizu, K. K., Holderegger, R., & Widmer, A. (2017). Estimating genomic diversity and population differentiation – An empirical comparison of microsatellite and SNP variation in Arabidopsis halleri. BMC Genomics, 18, 69. https://doi.org/10.1186/s12864-016-3459-7
- Fotsing, S. F., Margoliash, J., Wang, C., Saini, S., Yanicky, R., Shleizer-Burko, S., Goren, A., & Gymrek, M. (2019). The impact of short tandem repeat variation on gene expression. Nature Genetics, 51, 1652–1659. https://doi.org/10.1038/s41588-019-0521-9
- Gaggiotti, O. E., Bekkevold, D., Jørgensen, H. B. H., Foll, M., Carvalho, G. R., Andre, C., & Ruzzante, D. E. (2009). Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: Atlantic herring as a case study. Evolution, 63(11), 2939–2951. https://doi.org/10.1111/j.1558-5646.2009.00779.x
- Gagnaire, P.-A., Broquet, T., Aurelle, D., Viard, F., Souissi, A., Bonhomme, F., Arnaud-Haond, S., & Bierne, N. (2015). Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era. Evolutionary Applications, 8, 769–786. https://doi.org/10.1111/eva.12288
- Galli, G., Solidoro, C., & Lovato, T. (2017). Marine heat waves Hazard 3D maps and the risk for low motility organisms in a warming Mediterranean Sea. Frontiers in Marine Science, 4, 136. https://doi.org/10.3389/fmars.2017.00136
- Gao, X., & Starmer, J. D. (2008). AWclust: Point-and-click software for non-parametric population structure analysis. BMC Bioinformatics, 9, 77. https://doi.org/10.1186/1471-2105-9-77
- Gardeström, J., Pereyra, R. T., & André, C. (2008). Characterization of six microsatellite loci in the Baltic blue mussel Mytilus trossulus and cross-species amplification in North Sea Mytilus edulis. Conservation Genetics, 9, 1003–1005. https://doi.org/10.1007/s10592-007-9432-x
- Gardner, J. P. A., Oyarzún, P. A., Toro, J. E., Wenne, R., & Zbawicka, M. (2021). Phylogeography of southern hemisphere blue mussels of the genus Mytilus: Evolution, biosecurity, aquaculture and food labelling. Oceanography and Marine Biology: Annual Reviews, 59, 139–232. https://doi.org/10.1201/9781003138846-3
- Gardner, J. P. A., & Palmer, N. L. (1998). Size-dependent, spatial and temporal genetic variation at a leucine aminopeptidase (LAP) locus among blue mussel (Mytilus galloprovincialis) populations along a salinity gradient. Marine Biology, 132, 275–281. https://doi.org/10.1007/s002270050393
- Gardner, J. P. A., Zbawicka, M., Westfall, K. M., & Wenne, R. (2016). Invasive blue mussels threaten regional scale genetic diversity in mainland and remote offshore locations: The need for baseline data and enhanced protection in the Southern Ocean. Global Change Biology, 22, 3182–3195. https://doi.org/10.1111/gcb.13332
- Geller, J. B. (1999). Decline of a native mussel masked by sibling species invasion. Conservation Biology, 13, 661–664. https://doi.org/10.1046/j.1523-1739.1999.97470.x
- Gerdol, M., Moreira, R., Cruz, F., Gómez-Garrido, J., Vlasova, A., Rosani, U., Venier, P., Naranjo-Ortiz, M. A., Murgarella, M., Greco, S., Balseiro, P., Corvelo, A., Frias, L., Gut, M., Gabaldón, T., Pallavicini, A., Canchaya, C., Novoa, B., Alioto, T. S., … Figueras, A. (2020). Massive gene presence-absence variation shapes an open pan-genome in the Mediterranean mussel. Genome Biology, 21, 275. https://doi.org/10.1186/s13059-020-02180-3
- Giantsis, I. A., Mucci, N., Randi, E., Abatzopoulos, T. J., & Apostolidis, A. P. (2014). Microsatellite variation of mussels (Mytilus galloprovincialis) in central and eastern Mediterranean: Genetic panmixia in the Aegean and the Ionian seas. Journal of the Marine Biological Association of the United Kingdom, 94(4), 797–809. https://doi.org/10.1017/S0025315414000174
- Gruber, M. A. M., Hoffmann, B. D., Ritchie, P. A., & Lester, P. J. (2013). The conundrum of the yellow crazy ant (Anoplolepis gracilipes) reproductive mode: no evidence for dependent lineage genetic caste determination. Insectes Sociaux, 60, 135–145. https://doi.org/10.1007/s00040-012-0277-z
- Halpin, P. M., Sorte, C. J., Hofmann, G. E., & Menge, B. A. (2002). Patterns of variation in levels of Hsp70 in natural rocky shore populations from microscales to mesoscales. Integrative and Comparative Biology, 42(4), 815–824. https://doi.org/10.1093/icb/42.4.815
- Hamer, B., Jakšić, Ž., Pavičić-Hamer, D., Perić, L., Medaković, D., Ivanković, D., Pavičić, J., Zilberberg, C., Schröder, H. C., Müller, W. E. G., Smodlaka, N., & Batel, R. (2008). Effect of hypoosmotic stress by low salinity acclimation of Mediterranean mussels Mytilus galloprovincialis on biological parameters used for pollution assessment. Aquatic Toxicology, 89, 137–151. https://doi.org/10.1016/j.aquatox.2008.06.015
- Hamilton, J. S. (2019). Using neutral and outlier loci to uncover the genetic structure of Mytilus galloprovincialis populations from the eastern Adriatic coast using population genetic and seascape genetic approaches. MSc thesis. Victoria University of Wellington. http://researcharchive.vuw.ac.nz/handle/10063/8161
- Harley, C. D. G., Hughes, A. R., Hultgren, K. M., Miner, B. G., Sorte, C. J. B., Thomber, C. S., Rodriguez, L. F., Tomanek, L., & Williams, S. L. (2006). The impacts of climate change in coastal marine systems. Ecology Letters, 9, 228–241. https://doi.org/10.1111/j.1461-0248.2005.00871.x
- Hedgecock, D., Li, G., Hubert, S., Bucklin, K., & Ribes, V. (2004). Widespread null alleles and poor cross-species amplification of microsatellite DNA loci cloned from the Pacific oyster, Crassostrea gigas. Journal of Shellfish Research, 23(2), 379–385.
- Hilbish, T. J., Deaton, L. E., & Koehn, R. K. (1982). Effect of an allozyme polymorphism on regulation of cell volume. Nature, 298, 688–689. https://doi.org/10.1038/298688a0
- Hilbish, T. J., & Koehn, R. K. (1985). Dominance in physiological phenotypes and fitness at an enzyme locus. Science, 229, 52–54. https://doi.org/10.1126/science.4012310
- Hill, W. G. (1981). Estimation of effective population size from data on linkage disequilibrium. Genetical Research Cambridge, 38, 209–216. https://doi.org/10.1017/S0016672300020553
- Holderegger, R., Kamm, U., & Gugerli, F. (2006). Adaptive vs. neutral genetic diversity: Implications for landscape genetics. Landscape Ecology, 21, 797–807. https://doi.org/10.1007/s10980-005-5245-9
- IOR. (2022). Database of the sea bathing water quality in Croatia. Developed by Institute for Oceanography and Fisheries. Retrieved October, 2, 2010 from: https://vrtlac.izor.hr/ords/kakvoca/kakvoca_detalji10
- Jones, H. R., Johnson, K. M., & Kelly, M. W. (2019). Synergistic effects of temperature and salinity on the gene expression and physiology of Crassostrea virginica. Integrative and Comparative Biology, 59(2), 306–319. https://doi.org/10.1093/icb/icz035
- Kalinowski, S. T. (2005). HP-RARE 1.0: A computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes, 5, 187–189. https://doi.org/10.1111/j.1471-8286.2004.00845.x
- Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics Methods and Protocols, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
10.1093/bioinformatics/bts199 Google Scholar
- Kovačić, I., Pavičić-Hamer, D., Kanduč, T., & Hamer, B. (2017). Adaptation of cultured mussel Mytilus galloprovincialis Lamarck, 1819 from the northern Adriatic Sea to nearby aquaculture sites and translocation. Acta Adriatica, 58(2), 285–296. https://doi.org/10.32582/aa.58.2.8
- Krivokapić, S., Pestorić, B., Bosak, S., Kušpilić, G., & Wexels Riser, C. (2011). Trophic state of Boka Kotorska Bay (South-Eastern Adriatic Sea). Fresenius Environmental Bulletin, 20(8), 1960–1969.
- Larraín, M. A., Díaz, N. F., Lamas, C., Uribe, C., Jilberto, F., & Araneda, C. (2015). Heterologous microsatellite-based genetic diversity in blue mussel (Mytilus chilensis) and differentiation among localities in southern Chile. Latin American Journal of Aquatic Research, 43(5), 998–1010. https://doi.org/10.3856/vol43-issue5-fulltext-20
- Lejeusne, C., Chevaldonné, P., Pergent-Martini, C., Boudouresque, C. F., & Pérez, T. (2010). Climate change effects on a miniature ocean: The highly diverse, highly impacted Mediterranean Sea. Trends in Ecology and Evolution, 25(4), 250–260. https://doi.org/10.1016/j.tree.2009.10.009
- Liang, H., Zhang, Q., Lu, J., Yang, G., Tian, N., Wang, X., Tan, Y., & Tan, D. (2016). MSX2 induces trophoblast invasion in human placenta. PLoS One, 11(4), e0153656. https://doi.org/10.1371/journal.pone.0153656
- Lipizer, M., Partescano, E., Rabitti, A., Giorgetti, A., & Crise, A. (2014). Qualified temperature, salinity and dissolved oxygen climatologies in a changing Adriatic Sea. Ocean Science, 10, 771–797. https://doi.org/10.5194/os-10-771-2014
- Lockwood, B. L., Connor, K. M., & Gracey, A. Y. (2015). The environmentally tuned transcriptomes of Mytilus mussels. The Journal of Experimental Biology, 218, 1822–1833. https://doi.org/10.1242/jeb.118190
- Logan, C. A., Kost, L. E., & Somero, G. N. (2012). Latitudinal differences in Mytilus californianus thermal physiology. Marine Ecology Progress Series, 450, 93–105. https://doi.org/10.3354/meps09491
- Lupo, C., Bougeard, S., Le Bihan, V., Blin, J. L., Allain, G., Azéma, P., Benoit, F., Béchemin, C., Bernard, I., Blachier, P., Brieau, L., Danion, M., Garcia, A., Gervasoni, E., Glize, P., Lainé, A., Lapègue, S., Mablouké, C., Poirier, L., … Le Bouquin, S. (2021). Mortality of marine mussels Mytilus edulis and M. galloprovincialis: Systematic literature review of risk factors and recommendations for future research. Reviews in Aquaculture, 13(1), 504–536. https://doi.org/10.1111/raq.12484
- Mandić, M., Ikica, Z., & Gvozdenović, S. (2017). Mariculture in the Boka Kotorska Bay: Tradition, current state and perspective. In A. Joksimović, M. Djurović, A. V. Semenov, I. S. Zonn, & A. G. Kostianoy (Eds.), The Boka Kotorska Bay Environment (pp. 395–409). Springer. https://doi.org/10.1007/698_2016_33
- Manel, S., Schwartz, M. K., Luikart, G., & Taberlet, P. (2003). Landscape genetics: Combining landscape ecology and population genetics. Trends in Ecology and Evolution, 18(4), 189–197. https://doi.org/10.1016/S0169-5347(03)00008-9
- Michaelidis, B., Pörtner, H.-O., Sokolova, I., & Tomanek, L. (2014). Advances in predicting the impacts of global warming on the mussels Mytilus galloprovincialis in the Mediterranean Sea. In S. Goffredo & Z. Dubinsky (Eds.), The Mediterranean Sea: Its history and present challenges (pp. 319–339). Springer. https://doi.org/10.1007/978-94-007-6704-1_18
10.1007/978-94-007-6704-1_18 Google Scholar
- Moisiu, L., Panagiotopoulos, I. P., Durmishi, Ҫ., Kapsimalis, V., & Anagnostou, C. (2016). The anoxic Butrint Lagoon, SW Albania. Environmental Earth Sciences, 75, 1443. https://doi.org/10.1007/s12665-016-6259-0
- Negri, A., Oliveri, C., Sforzini, S., Mignione, F., Viarengo, A., & Banni, M. (2013). Transcriptional response of the mussel Mytilus galloprovincialis (lam.) following exposure to heat stress and copper. PLoS One, 8(6), e66802. https://doi.org/10.1371/journal.pone.0066802
- Oliver, E. C. J., Donat, M. G., Burrows, M. T., Moore, P. J., Smale, D. A., Alexander, L. V., Benthuysen, J. A., Feng, M., Gupta, A. S., Hobday, A. J., Holbrook, N. J., Perkins-Kirkpatrick, S. E., Scannell, H. A., Straub, S. C., & Wernberg, T. (2018). Longer and more frequent marine heatwaves over the past century. Nature Communications, 9, 1324. https://doi.org/10.1038/s41467-018-03732-9
- Pascual, M., Rives, B., Schunter, C., & MacPherson, E. (2017). Impact of life history traits on gene flow: A multispecies systematic review across oceanographic barriers in the Mediterranean Sea. PLoS One, 12(5), e0176419. https://doi.org/10.1371/journal.pone.0176419
- Paterno, M., Bat, L., Souissi, J. B., Boscari, E., Chassanite, A., Congiu, L., Guarnieri, G., Kruschel, C., Mačić, V., Marino, I. A. M., Micu, D., Milchakova, N., Panayotova, M., Papetti, C., Planes, S., Strungaru, S., Todorova, V. R., Voutsinas, E., & Zane, L. (2019). A genome-wide approach to the phylogeography of the mussel Mytilus galloprovincialis in the Adriatic and the black seas. Frontiers in Marine Science, 6, 566. https://doi.org/10.3389/fmars.2019.00566
- Peakall, R., & Smouse, P. E. (2012). GenAlEx 6.5: Genetic analysis in excel. Population genetic structure for teaching and research – An update. Bioinformatics, 28, 2537–2539. https://doi.org/10.1093/bioinformatics/bts460
- Pechenik, J. A. (1999). On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Marine Ecology Progress Series, 177, 269–297. https://doi.org/10.3354/meps177269
- Presa, P., Pérez, M., & Diz, A. P. (2002). Polymorphic microsatellite markers for blue mussels (Mytilus spp.). Conservation Genetics, 3, 441–443. https://doi.org/10.1023/A:1020571202907
- Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. https://doi.org/10.1093/genetics/155.2.945
- R Core Team. (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing http://www.R-project.org/
- Ramón, M., Fernández, M., & Galimany, E. (2007). Development of mussel (Mytilus galloprovincialis) seed from two different origins in a semi-enclosed Mediterranean Bay (N.E. Spain). Aquaculture, 264, 148–159. https://doi.org/10.1016/j.aquaculture.2006.11.014
- Riginos, C., & Liggins, L. (2013). Seascape genetics: Populations, individuals, and genes marooned and adrift. Geography Compass, 7(3), 197–216. https://doi.org/10.1111/gec3.12032
10.1111/gec3.12032 Google Scholar
- Rioux Paquette, S. (2011). PopGenKit: Useful function for (batch) file conversion and data resampling in microsatellite datasets. R package.
- Rousset, F. (2008). GENEPOP ‘007: A complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources, 8(1), 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
- Saarman, N. P., Kober, K. M., Simison, W. B., & Pogson, G. H. (2017). Sequence-based analysis of thermal adaptation and protein energy landscapes in an invasive blue mussel (Mytilus galloprovincialis). Genome Biology and Evolution, 9(10), 2739–2751. https://doi.org/10.1093/gbe/evx190
- Schmidt, P. S., Serrão, E. A., Pearson, G. A., Riginos, C., Rawson, P. D., Hilbish, T. J., Brawley, S. H., Trussell, G. C., Carrington, E., Wethey, D. S., Grahame, J. W., Bonhomme, F., & Rand, D. M. (2008). Ecological genetics In the North Atlantic: Environmental gradients and adaptation At specific loci. Ecology, 89(11), S91–S107. https://doi.org/10.1890/07-1162.1
- Schneider, K. R., & Helmuth, B. (2007). Spatial variability in habitat temperature may drive patterns of selection between an invasive and native mussel species. Marine Ecology Progress Series, 339, 157–167. https://doi.org/10.3354/meps339157
- SeaDataNet.org. Originally accessed at http://sdn.oceanbrowser.net/web-vis/ and http://gher-diva.phys.ulg.ac.be/emodnet/ accessed 28/10/2018. Now available at https://www.seadatanet.org/Products#/metadata/2a2aa0c5-4054-4a62-a18b-3835b304fe64.
- Segovia, N. I., González-Wevar, C. A., & Haye, P. A. (2020). Signatures of local adaptation in the spatial genetic structure of the ascidian Pyura chilensis along the Southeast Pacific coast. Scientific Reports, 10, 14098. https://doi.org/10.1038/s41598-020-70798-1
- Selkoe, K. A., D'Aloia, C. C., Crandall, E. D., Iacchei, M., Liggins, L., Puritz, J. B., von der Heyden, S., & Toonen, R. J. (2016). A decade of seascape genetics: Contributions to basic and applied marine connectivity. Marine Ecology Progress Series, 554, 1–19. https://doi.org/10.3354/meps11792
- Selkoe, K. A., Gaines, S. D., Caselle, J. E., & Warner, R. R. (2006). Current shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology, 87, 3082–3094. https://doi.org/10.1890/0012-9658(2006)87[3082:csakae]2.0.co;2
- Selkoe, K. A., Scribner, K. T., & Galindo, H. M. (2015). Waterscape genetics: Applications of landscape genetics to rivers, lakes, and seas. In N. Balkenhol, S. A. Cushman, A. T. Storfer, & L. P. Waits (Eds.), Landscape genetics (pp. 220–246). Wiley Blackwell, West Sussex. https://doi.org/10.1002/9781118525258.ch13
10.1002/9781118525258.ch13 Google Scholar
- Silva, C. N. S., & Gardner, J. P. A. (2016). Identifying environmental factors associated with the genetic structure of the New Zealand scallop: Linking seascape genetics and ecophysiological tolerance. ICES Journal of Marine Science, 73(7), 1925–1934. https://doi.org/10.1093/icesjms/fsv240
- Štambuk, A., Šrut, M., Šatović, Z., Tkalec, M., & Klobučar, G. I. V. (2013). Gene flow vs. pollution pressure: Genetic diversity of Mytilus galloprovincialis in eastern Adriatic. Aquatic Toxicology, 136-137, 22–31. https://doi.org/10.1016/j.aquatox.2013.03.017
- Tomanek, L. (2012). Environmental proteomics of the mussel Mytilus: Implications for tolerance to stress and change in limits of biogeographical ranges in response to climate change. Integrative and Comparative Biology, 52(5), 648–664. https://doi.org/10.1093/icb/ics114
- Tomanek, L., & Helmuth, B. (2002). Physiological ecology of rocky intertidal organisms: A synergy of concepts. Integrative and Comparative Biology, 42, 771–775. https://doi.org/10.1093/icb/42.4.771
- UNEP/MAP-RAC/SPA. (2015). Adriatic Sea: Description of the ecology and identification of the areas that may deserve to be protected. By Cerrano C. Edited by Cebrian D and Requena S. RAC/SPA, Tunis.
- Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., & Shipley, P. (2004). Micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
- Vaux, F., Bohn, S., Hyde, J. R., & O'Malley, K. G. (2021). Adaptive markers distinguish north and South Pacific albacore amid low population differentiation. Evolutionary Applications, 14(5), 1343–1364. https://doi.org/10.1111/eva.13202
- Verdura, J., Linares, C., Ballesteros, E., Coma, R., Uriz, M. J., Bensoussan, N., & Cebrian, E. (2019). Biodiversity loss in a Mediterranean ecosystem due to an extreme warming event unveils the role of an engineering gorgonian species. Scientific Reports, 9(1), 5911. https://doi.org/10.1038/s41598-019-41929-0
- Verhoeven, K. J. F., Simonsen, K. L., & McIntyre, L. M. (2005). Implementing false discovery rate control: Increasing your power. Oikos, 3, 643–647. https://doi.org/10.1111/j.0030-1299.2005.13727.x
- Waits, L. P., & Storfer, A. (2015). Basics of population genetics: Quantifying neutral and adaptive genetic variation for landscape genetic studies. In N. Balkenhol, S. A. Cushman, A. T. Storfer, & L. P. Waits (Eds.), Landscape genetics (pp. 35–57). Wiley Blackwell, West Sussex. https://doi.org/10.1002/9781118525258.ch03
10.1002/9781118525258.ch03 Google Scholar
- Waples, R. S. (2006). A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked loci. Conservation Genetics, 7(2), 167–184. https://doi.org/10.1007/s10592-005-9100-y
- Waples, R. S., & Do, C. (2010). Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: A largely untapped resource for applied conservation and evolution. Evolutionary Applications, 3(3), 244–262. https://doi.org/10.1111/j.1752-4571.2009.00104.x
- Wei, K.-J., Wood, A. R., & Gardner, J. P. A. (2013a). Seascape genetics of the New Zealand greenshell mussel: Sea surface temperature explains macrogeographic scale genetic variation. Marine Ecology Progress Series, 477, 107–121. https://doi.org/10.3354/meps10158
- Wei, K.-J., Wood, A. R., & Gardner, J. P. A. (2013b). Population genetic variation in the New Zealand greenshell mussel: Locus-dependent conflicting signals of weak structure and high gene flow balanced against pronounced structure and high self-recruitment. Marine Biology, 160, 931–949. https://doi.org/10.1007/s00227-012-2145-9
- Wenne, R., Zbawicka, M., Bach, L., Strelkov, P., Gantsevich, M., Kuklinski, P., Kijewski, T., McDonald, J. H., Sundsaasen, K. K., Árnyasi, M., Lien, S., Kaasik, A., Herkül, K., & Kotta, J. (2020). Trans-Atlantic distribution and introgression as inferred from single nucleotide polymorphism: Mussels mytilus and environmental factors. Genes, 11(5), 530. https://doi.org/10.3390/genes11050530
- Wenne, R., Zbawicka, M., Prądzińska, A., Kotta, J., Herkül, K., Gardner, J. P. A., Apostolidis, A. P., Poćwierz-Kotus, A., Rouane-Hacene, O., Korrida, A., Dondero, F., Baptista, M., Reizopoulou, S., Hamer, B., Sundsaasen, K. K., Árnyasi, M., & Kent, M. P. (2022). Molecular genetic differentiation of native populations of Mediterranean blue mussels, Mytilus galloprovincialis (Lamarck, 1819), and the relationship with environmental variables. European Zoological Journal, 89, 755–784.
- Westfall, K. M. (2011). Molecular ecology and systematics of blue mussels (genus Mytilus) (Mytilidae; Bivalvia; Mollusca) in the southern hemisphere. PhD thesis. Victoria University of Wellington.
- White, T. A., Stamford, J., & Hoelzel, A. R. (2010). Local selection and population structure in a deep-sea fish, the roundnose grenadier (Coryphaenoides rupestris). Molecular Ecology, 19, 216–226. https://doi.org/10.1111/j.1365-294X.2009.04446.x
- Wu, Z., Gong, H., Zhang, M., Tong, X., Ai, H., Xiao, S., Perez-Enciso, M., Yang, B., & Huang, L. (2021). A worldwide map of swine short tandem repeats and their associations with evolutionary and environmental adaptations. Genetics Selection Evolution, 53(1), 39. https://doi.org/10.1186/s12711-021-00631-4
- Yu, H., & Li, Q. (2007). Development of EST-SSRs in the Mediterranean mussel, Mytilus galloprovincialis. Molecular Ecology Notes, 7, 1308–1310. https://doi.org/10.1111/j.1471-8286.2007.01865.x
- Zbawicka, M., Wenne, R., & Burzyński, A. (2014). Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels. Molecular Genetics and Genomics, 289, 1275–1287. https://doi.org/10.1007/s00438-014-0888-3
- Zeng, C., Rowden, A. A., Clark, M. R., & Gardner, J. P. A. (2020). Species-specific genetic variation in response to deep-sea environmental variation amongst vulnerable marine ecosystem indicator taxa. Scientific Reports, 10, 2844. https://doi.org/10.1038/s41598-020-59210-0
- Zonn, I. S., & Kostianoy, A. G. (2017). The Adriatic Sea. In A. Joksimović, M. Djurović, A. V. Semenov, I. S. Zonn, & A. G. Kostianoy (Eds.), The Boka Kotorska Bay Environment (pp. 19–41). Springer. https://doi.org/10.1007/698_2016_42
- Zouros, E., & Foltz, D. W. (1984). Possible explanations of heterozygote deficiency in bivalve Molluscs. Malacologia, 25(2), 583–591.
