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Genetic diversity of Ponto-Caspian amphipods throughout the invaded Baltic and native NW Black Sea donor ranges: does introduction mode matter?

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Abstract

The SE Baltic region harbors a diverse assemblage of alien amphipods of Ponto-Caspian origin. The composition of this fauna was shaped by three invasion waves: (1) pre-twentieth century dispersals via watershed-connecting canals, (2) deliberate introductions in the 1960s, and (3) last decade dispersals via shipping and existing canals. Given this complex history, we test whether genetic diversity (mitochondrial COI and nuclear OPS) differs between the native and invaded ranges and between the deliberately introduced species and the ones that dispersed on their own. We find that in the native range the two species groups exhibited similar COI diversity, while OPS diversity was higher in the deliberately introduced species. In the invaded range, COI diversity significantly decreased in all species, but more so in the self-dispersed group. No change in OPS diversity was detected among ranges. Mitochondrial diversity was more structured geographically in the native range, and the dominant invasive haplotypes were detected in the native populations of all but one species, further highlighting the utility of this marker in tracing invasion sources. Our comparative approach provides important insight into the inter-range genetic diversity of Ponto-Caspian invaders, highlighting the role of introduction mode.

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Data availability

The DNA sequences generated during this study are available in GenBank (COI: OQ788623-OQ788975, OPS: OQ813899-OQ81405, 28S: OQ801263-OQ801288).

References

  • Arbačiauskas, K., 2008. Amphipods of the Nemunas river and the Curonian lagoon, the Baltic Sea basin: where and which native freshwater amphipods persist? Acta Zoologica Lituanica 18: 10–16.

    Article  Google Scholar 

  • Arbačiauskas, K., G. Višinskienė, S. Smilgevičienė & V. Rakauskas, 2011. Non-indigenous macroinvertebrate species in Lithuanian fresh waters, part 1: distributions, dispersal and future. Knowledge and Management of Aquatic Ecosystems 402: 12.

    Article  Google Scholar 

  • Arbačiauskas, K., J. Lesutienė & Z. R. Gasiūnaitė, 2013. Feeding strategies and elemental composition in Ponto-Caspian peracaridans from contrasting environments: can stoichiometric plasticity promote invasion success? Freshwater Biology 58: 1052–1068.

    Article  Google Scholar 

  • Arbačiauskas, K., E. Šidagytė, V. Šniaukštaitė & J. Lesutienė, 2017. Range expansion of Ponto-Caspian peracaridan Crustaceans in the Baltic sea basin and its aftermath: Lessons from Lithuania. Aquatic Ecosystem Health and Management 20: 393–401.

    Google Scholar 

  • Astrin, J. J. & P. E. Stüben, 2008. Phylogeny in cryptic weevils: molecules, morphology and new genera of western Palaearctic Cryptorhynchinae (Coleoptera:Curculionidae). Invertebrate Systematics 22: 503–522.

    Article  Google Scholar 

  • Audzijonyte, A., M. E. Daneliya, N. Mugue & R. Väinölä, 2008. Phylogeny of Paramysis (Crustacea: Mysida) and the origin of Ponto-Caspian endemic diversity: resolving power from nuclear protein-coding genes. Molecular Phylogenetics and Evolution 46: 738–759.

    Article  CAS  PubMed  Google Scholar 

  • Audzijonyte, A., K. J. Wittmann, I. Ovcarenko & R. Väinölä, 2009. Invasion phylogeography of the Ponto-Caspian crustacean Limnomysis benedeni dispersing across Europe. Diversity and Distributions 15: 346–355.

    Article  Google Scholar 

  • Audzijonyte, A., L. Baltrūnaitė, R. Väinölä & K. Arbačiauskas, 2015. Migration and isolation during the turbulent Ponto-Caspian Pleistocene create high diversity in the crustacean Paramysis lacustris. Molecular Ecology 24: 4537–4555.

    Article  PubMed  Google Scholar 

  • Audzijonyte, A., L. Baltrūnaitė, R. Väinölä & K. Arbačiauskas, 2017. Human-mediated lineage admixture in an expanding Ponto-Caspian crustacean species Paramysis lacustris created a novel genetic stock that now occupies European waters. Biological Invasions 19: 2443–2457.

    Article  Google Scholar 

  • Baker, H. G. & G. L. Stebbins, 1965. The Genetics of Colonizing Species, Academic, New York:

    Google Scholar 

  • Bates, D., M. Mächler, B. Bolker & S. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.

    Article  Google Scholar 

  • Breheny, P. & W. Burchett, 2017. Visualization of regression models using visreg. The R Journal 9: 56.

    Article  Google Scholar 

  • Bridle, J. R. & T. H. Vines, 2007. Limits to evolution at range margins: when and why does adaptation fail? Trends in Ecology & Evolution 22: 140–147.

    Article  Google Scholar 

  • Colautti, R. I. & J. A. Lau, 2015. Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Molecular Ecology 24: 1999–2017.

    Article  PubMed  Google Scholar 

  • Copilaş-Ciocianu, D. & E. Šidagytė-Copilas, 2022. A substantial range expansion of alien Ponto-Caspian amphipods along the eastern Baltic Sea coast. Oceanologia 64: 227–232.

    Article  Google Scholar 

  • Copilaş-Ciocianu, D. & D. Sidorov, 2022. Taxonomic, ecological and morphological diversity of Ponto-Caspian gammaroidean amphipods: a review. Organisms Diversity & Evolution 22: 285–315.

    Article  Google Scholar 

  • Copilaş-Ciocianu, D., T. Rewicz, A. F. Sands, D. Palatov, I. Marin, K. Arbačiauskas, P. D. N. Hebert, M. Grabowski & A. Audzijonyte, 2022a. A DNA barcode reference library for endemic Ponto-Caspian amphipods. Scientific Reports 12: 11332.

    Article  PubMed  PubMed Central  Google Scholar 

  • Copilaş-Ciocianu, D., A. Sarmanov, N. Sergaliyev & D. Sidorov, 2022b. Turcogammarus aralensis (Uljanin, 1875), a relict pontogammarid amphipod crustacean from the Aralo-Caspian paleobasin: redescription, phylogenetic position and biogeography. Zootaxa 5219: 101–120.

    Article  PubMed  Google Scholar 

  • Copilaş-Ciocianu, D., D. Sidorov & E. Šidagytė-Copilas, 2023. Global distribution and diversity of alien Ponto-Caspian amphipods. Biological Invasions 25: 179–195.

    Article  Google Scholar 

  • Cristescu, M. E. A. & P. D. N. Hebert, 2005. The “Crustacean seas” - An evolutionary perspective on the Ponto-Caspian peracarids. Canadian Journal of Fisheries and Aquatic Sciences 62: 505–517.

    Article  Google Scholar 

  • Cristescu, M. E. A., P. D. N. Hebert, J. D. S. Witt, H. J. MacIsaac & I. A. Grigorovich, 2001. An invasion history for Cercopagis pengoi based on mitochondrial gene sequences. Limnology and Oceanography 46: 224–229.

    Article  Google Scholar 

  • Cristescu, M. E. A., J. D. S. Witt, I. A. Grigorovich, P. D. N. Hebert & H. J. MacIsaac, 2004. Dispersal of the Ponto-Caspian amphipod Echinogammarus ischnus: Invasion waves from the Pleistocene to the present. Heredity 92: 197–203.

    Article  CAS  PubMed  Google Scholar 

  • Cuthbert, R. N., S. G. Kotronaki, J. T. A. Dick & E. Briski, 2020. Salinity tolerance and geographical origin predict global alien amphipod invasions. Biology Letters Royal Society Publishing 16: 20200354.

    Google Scholar 

  • de Vaate Bij, A., K. Jazdzewski, H. A. M. Ketelaars, S. Gollasch & G. van der Velde, 2002. Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 59: 1159–1174.

    Article  Google Scholar 

  • Dermott, R., J. Witt, Y. M. Um & M. González, 1998. Distribution of the Ponto-Caspian amphipod Echinogammarus ischnus in the great lakes and replacement of native Gammarus fasciatus. Journal of Great Lakes Research 24: 442–452.

    Article  Google Scholar 

  • Dlugosch, K. M., S. R. Anderson, J. Braasch, F. A. Cang & H. D. Gillette, 2015. The devil is in the details: genetic variation in introduced populations and its contributions to invasion. Molecular Ecology 24: 2095–2111.

    Article  PubMed  Google Scholar 

  • Edgar, R. C., 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estoup, A., V. Ravigné, R. Hufbauer, R. Vitalis, M. Gautier & B. Facon, 2016. Is there a genetic paradox of biological invasion? Annual Review of Ecology, Evolution, and Systematics 47: 51–72.

    Article  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Fu, Y.-X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gasiūnas, I., 1963. The acclimatization of fodder crustaceans (of the Caspian relict type) into the reservoir of Kaunas Hydroelectric power station and the possibility of their transference into other water bodies. LTSR MA Darbai, Serija C 1(30): 79–85.

    Google Scholar 

  • Gasiūnas, I., 1972. Obogoschenie kormovoj bazy ryb vodoemov Litvy akklimatizirovannymi rakoobraznymi Kaspijskogo kompleksa. (Enrichment of fodder basis of water bodies of Lithuania by acclimatized crustaceans-like organisms from the Caspian Sea complex. In Russian). In: J. Maniukas, J. Virbickas (Eds.), Voprosy razvedenija ryb I rakoobraznykh v vodoemakh Litvy (On the breeding of fish and crustacean-like organisms in the water bodies of Lithuania), pp. 57–68. Mintis, Vilnius, Lithuania.

  • Grabowski, M., K. Bacela, A. Konopacka & K. Jazdzewski, 2009. Salinity-related distribution of alien amphipods in rivers provides refugia for native species. Biological Invasions 11: 2107–2117.

    Article  Google Scholar 

  • Grabowski, M., T. Rewicz, K. Bacela-Spychalska, A. Konopacka, T. Mamos & K. Jazdzewski, 2012. Cryptic invasion of baltic lowlands by freshwater amphipod of Pontic origin. Aquatic Invasions 7(3): 337–346.

    Article  Google Scholar 

  • Grudule, N., E. Parele & K. Arbačiauskas, 2007. Distribution of Ponto-Caspian amphipod Pontogammarus robustoides in Latvian waters. Acta Zoologica Lituanica 17: 28–32.

    Article  Google Scholar 

  • Guo, W., S. Qiao, Y. Wang, S. Shi, F. Tan & Y. Huang, 2015. Genetic diversity, population structure, and genetic relatedness of native and non-native populations of Spartina alterniflora (Poaceae, Chloridoideae). Hydrobiologia 745: 313–327.

    Article  CAS  Google Scholar 

  • Hardie, D. C. & J. A. Hutchings, 2010. Evolutionary ecology at the extremes of species’ ranges. Environmental Reviews 18: 1–20.

    Article  Google Scholar 

  • Harpending, H. C., 1994. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66: 591–600.

    CAS  PubMed  Google Scholar 

  • Haubrock, P. J., R. N. Cuthbert, A. Ricciardi, C. Diagne & F. Courchamp, 2022. Economic costs of invasive bivalves in freshwater ecosystems. Diversity and Distributions 28: 1010–1021.

    Article  Google Scholar 

  • Hill, J. K., H. M. Griffiths & C. D. Thomas, 2011. Climate change and evolutionary adaptations at species’ range margins. Annual Review of Entomology 56: 143–159.

    Article  CAS  PubMed  Google Scholar 

  • Hou, Z., J. Fu & S. Li, 2007. A molecular phylogeny of the genus Gammarus (Crustacea: Amphipoda) based on mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution 45: 596–611.

    Article  CAS  PubMed  Google Scholar 

  • Hou, Z., B. Sket & S. Li, 2014. Phylogenetic analyses of Gammaridae crustacean reveal different diversification patterns among sister lineages in the Tethyan region. Cladistics 30: 352–365.

    Article  PubMed  Google Scholar 

  • Hupało, K., H. W. Riss, M. Grabowski, J. Thiel, K. Bącela-Spychalska & E. I. Meyer, 2018. Climate change as a possible driver of invasion and differential in HSP70 expression in two genetically distinct populations of the invasive killer shrimp, Dikerogammarus villosus. Biological Invasions 20: 2047–2059.

    Article  Google Scholar 

  • Hupało, K., D. Copilaş-Cioianu, F. Leese & M. Weiss, 2023. Morphology, nuclear SNPs and mate selection reveal that COI barcoding overestimates species diversity in a Mediterranean freshwater amphipod by an order of magnitude. Cladistics 39: 129–143.

    Article  PubMed  Google Scholar 

  • Jarocki, J., & A. Demianowicz, 1931. Über das Vorkommen des ponto-kaspischen Amphipoden Chaetogammarus tenellus (G.O.Sars) in der Wisla (Weichsel). Bull Int Acad Pol Sci Lett, Cl Math Nat Ser B(II) 2: 513–530.

  • Jażdżewski, K., 1980. Range extensions of some Gammaridean species in European inland waters caused by human activity. Crustaceana. Supplement 6: 84–107.

    Google Scholar 

  • Jażdżewska, A. M., T. Rewicz, T. Mamos, R. Wattier, K. Bącela-Spychalska & M. Grabowski, 2020. Cryptic diversity and mtDNA phylogeography of the invasive demon shrimp, Dikerogammarus haemobaphes (Eichwald, 1841), in Europe. NeoBiota 57: 53–86.

    Article  Google Scholar 

  • Jeffery, N. W., L. Yampolsky & T. R. Gregory, 2017. Nuclear DNA content correlates with depth, body size, and diversification rate in amphipod crustaceans from ancient Lake Baikal, Russia. Genome 60: 303–309.

    Article  CAS  PubMed  Google Scholar 

  • Kao, D., A. G. Lai, E. Stamataki, S. Rosic, N. Konstantinides, E. Jarvis, A. di Donfrancesco, N. Pouchkina-Stancheva, M. Sémon, M. Grillo, H. Bruce, S. Kumar, I. Siwanowicz, A. Le, A. Lemire, M. B. Eisen, C. Extavour, W. E. Browne, C. Wolff, M. Averof, N. H. Patel, P. Sarkies, A. Pavlopoulos, & A. Aboobaker, 2016. The genome of the crustacean Parhyale hawaiensis, a model for animal development, regeneration, immunity and lignocellulose digestion. eLife 5: e20062.

  • Kolbe, J. J., R. E. Glor, L. R. Schettina, A. C. Lara, A. Larson & J. B. Losos, 2007. Multiple sources, admixture, and genetic variation in introduced anolis lizard populations. Conservation Biology 21: 1612–1625.

    Article  PubMed  Google Scholar 

  • Krijgsman, W., A. Tesakov, T. Yanina, S. Lazarev, G. Danukalova, C. G. C. van Baak, J. Agustí, M. C. Alçiçek, E. Aliyeva, D. Bista, A. Bruch, Y. Büyükmeriç, M. Bukhsianidze, R. Flecker, P. Frolov, T. M. Hoyle, E. L. Jorissen, U. Kirscher, S. A. Koriche, S. B. Kroonenberg, D. Lordkipanidze, O. Oms, L. Rausch, J. Singarayer, M. Stoica, S. van de Velde, V. V. Titov & F. P. Wesselingh, 2019. Quaternary time scales for the Pontocaspian domain: Interbasinal connectivity and faunal evolution. Earth-Science Reviews 188: 1–40.

    Article  Google Scholar 

  • Kuznetsova, A., P. B. Brockhoff & R. H. B. Christensen, 2017. lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82: 1–26.

    Article  Google Scholar 

  • Lenth, R. V., 2022. emmeans: Estimated marginal means, aka least-squares means. R package version 1.7.5. https://CRAN.R-project.org/package=emmeans.

  • Lipinskaya, T., A. Makaranka, V. Razlutskij & V. Semenchenko, 2021. First records of the alien amphipod Dikerogammarus haemobaphes (Eichwald, 1841) in the Neman river basin (Belarus). BioInvasions Records 10: 319–325.

    Article  Google Scholar 

  • Meßner, U. & M. L. Zettler, 2018. The conquest (and avoidance?) of the brackish environment by Ponto-Caspian amphipods: a case study of the German Baltic Sea. BioInvasions Records 7: 269–278.

    Article  Google Scholar 

  • Meßner, U. & M. L. Zettler, 2021. Drastic changes of the amphipod fauna in northern Germany and the displacement of Gammarus lacustris G. O. Sars 1864 to relict habitats/status. Knowledge & Management of Aquatic Ecosystems 422: 17.

    Article  Google Scholar 

  • Minchin, D., K. Arbačiauskas, D. Daunys, E. Ezhova, N. Grudule, J. Kotta, N. Molchanova, S. Olenin, G. Višinskienė & S. Strake, 2019. Rapid expansion and facilitating factors of the Ponto-Caspian invader Dikerogammarus villosus within the Eastern Baltic sea. Aquatic Invasions 14: 165–181.

    Article  Google Scholar 

  • Moedt, S. & T. van Haaren, 2018. Pontogammarus robustoides (Sars, 1894), a new non-indigenous amphipod in the Netherlands (Crustacea: Amphipoda). Lauterbornia 85: 123–126.

    Google Scholar 

  • Morhun, H., D. Copilas-Ciocianu, T. Rewicz, M. O. Son, A. Khomenko, M. Huseynov, S. Utevsky & M. Grabowski, 2022. Molecular markers and SEM imaging reveal pseudocryptic diversity within the Ponto-Caspian low-profile amphipod invader Dikerogammarus bispinosus. European Zoological Journal 89: 87–101.

    Article  CAS  Google Scholar 

  • Moškrič, A. & R. Verovnik, 2019. Five nuclear protein-coding markers for establishing a robust phylogenetic framework of niphargid crustaceans (Niphargidae: Amphipoda) and new molecular sequence data. Data in Brief 25: 104134.

    Article  PubMed  PubMed Central  Google Scholar 

  • Paidere, J. & A. Brakovska, 2022. The Ponto-Caspian and native amphipod life history in the Daugava River, Latvia. Oceanological and Hydrobiological Studies 51: 268–282.

    Article  Google Scholar 

  • Paiva, F., A. Barco, Y. Chen, A. Mirzajani, F. T. Chan, V. Lauringson, M. Baltazar-Soares, A. Zhan, S. A. Bailey, J. Javidpour & E. Briski, 2018. Is salinity an obstacle for biological invasions? Global Change Biology 24: 2708–2720.

    Article  PubMed  Google Scholar 

  • Panov, V. E., B. Alexandrov, K. Arbačiauskas, R. Binimelis, G. H. Copp, M. Grabowski, F. Lucy, R. S. Leuven, S. Nehring, M. Paunović, V. Semenchenko & M. O. Son, 2009. Assessing the risks of aquatic species invasions via European inland waterways: from concepts to environmental indicators. Integrated Environmental Assessment and Management 5(1): 110–126.

    Article  CAS  PubMed  Google Scholar 

  • Ramos-Onsins, S. E. & J. Rozas, 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19: 2092–2100.

    Article  CAS  PubMed  Google Scholar 

  • Rees, D. J., F. Dufresne, H. Glémet & C. Belzile, 2007. Amphipod genome sizes: first estimates for Arctic species reveal genomic giants. Genome 50: 151–158.

    Article  CAS  PubMed  Google Scholar 

  • Reid, D. F. & M. I. Orlova, 2002. Geological and evolutionary underpinnings for the success of Ponto-Caspian species invasions in the Baltic Sea and North American Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 1144–1158.

    Article  Google Scholar 

  • Rewicz, T., M. Grabowski, C. MacNeil & K. Bącela-Spychalska, 2014. The profile of a ‘perfect’ invader – the case of killer shrimp, Dikerogammarus villosus. Aquatic Invasions 9: 267–288.

    Article  Google Scholar 

  • Rewicz, T., R. Wattier, M. Grabowski, T. Rigaud & K. Bącela-Spychalska, 2015. Out of the Black Sea: Phylogeography of the Invasive Killer Shrimp Dikerogammarus villosus across Europe. PLOS ONE 10: e0118121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rewicz, T., R. Wattier, T. Rigaud, M. Grabowski, T. Mamos & K. Bącela-Spychalska, 2017. The killer shrimp, Dikerogammarus villosus, invading European Alpine lakes: a single main source but independent founder events with an overall loss of genetic diversity. Freshwater Biology 62: 1036–1051.

    Article  CAS  Google Scholar 

  • Roman, J. & J. Darling, 2007. Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology & Evolution 22: 454–464.

    Article  Google Scholar 

  • Rozas, J., A. Ferrer-Mata, J. C. Sanchez-DelBarrio, S. Guirao-Rico, P. Librado, S. E. Ramos-Onsins & A. Sanchez-Gracia, 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34: 3299–3302.

    Article  CAS  PubMed  Google Scholar 

  • Salzburger, W., G. B. Ewing & A. von Haeseler, 2011. The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology 20: 1952–1963.

    Article  PubMed  Google Scholar 

  • Šidagytė, E. & K. Arbačiauskas, 2016. Resistance to low oxygen in the Ponto-Caspian amphipod Pontogammarus robustoides varies among lentic habitats of its northern invaded range. Limnologica 61: 7–13.

    Article  Google Scholar 

  • Šidagytė, E., S. Solovjova, V. Šniaukštaitė, A. Šiaulys, S. Olenin & K. Arbačiauskas, 2017. The killer shrimp Dikerogammarus villosus (Crustacea, Amphipoda) invades Lithuanian waters, South-Eastern Baltic Sea. Oceanologia 59: 85–91.

    Article  Google Scholar 

  • Soto, I., R. N. Cuthbert, D. A. Ahmed, A. Kouba, S. Domisch, J. R. G. Marquez, A. Beidas, G. Amatulli, J. Kiesel, L. Q. Shen, M. Florencio, H. Lima, E. Briski, F. Altermatt, G. Archambaud-Suard, P. Borza, Z. Csabai, T. Datry, M. Floury, M. Forcellini, J. Fruget, P. Leitner, M. Lizée, A. Maire, A. Ricciardi, R. B. Schäfer, R. Stubbington, G. H. van der Lee, G. Várbíró, R. C. M. Verdonschot, P. Haase & P. J. Haubrock, 2022. Tracking a killer shrimp: Dikerogammarus villosus invasion dynamics across Europe. Diversity and Distributions 29: 157–172.

    Article  Google Scholar 

  • Stephens, M., N. J. Smith & P. Donnelly, 2001. A new statistical method for haplotype reconstruction from population data. The American Journal of Human Genetics 68: 978–989.

    Article  CAS  PubMed  Google Scholar 

  • Stepien, C. A., J. E. Brown, M. E. Neilson & M. A. Tumeo, 2005. Genetic diversity of invasive species in the great lakes versus their Eurasian source populations: insights for risk analysis. Risk Analysis 25: 1043–1060.

    Article  PubMed  Google Scholar 

  • Strayer, D. L., 2009. Twenty years of zebra mussels: lessons from the mollusk that made headlines. Frontiers in Ecology and the Environment 7: 135–141.

    Article  Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi, Y., Y. Suyama, Y. Matsuki, R. Funayama, K. Nakayama & M. Kawata, 2016. Lack of genetic variation prevents adaptation at the geographic range margin in a damselfly. Molecular Ecology 25: 4450–4460.

    Article  PubMed  Google Scholar 

  • Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaitonis, G., L. Lazauskienė, & A. Razinkovas, 1990. Izuchenie rezul’tatov ekonomicheskoj effektivnosti i perspektivy akklimatizacii bezpozvonochnyh v vodoemah Pribaltiki (Study of economic efficiency and prospects of acclimatization of invertebrates in water bodies of the Baltic states). Vilnius.

  • Vanderploeg, H. A., T. F. Nalepa, D. J. Jude, E. L. Mills, K. T. Holeck, J. R. Liebig, I. A. Grigorovich & H. Ojaveer, 2002. Dispersal and emerging ecological impacts of Ponto-Caspian species in the Laurentian great lakes. Canadian Journal of Fisheries and Aquatic Sciences 59: 1209–1228.

    Article  Google Scholar 

  • Weiss, M., H. Weigand & F. Leese, 2022. Individual small in-stream barriers contribute little to strong local population genetic structure five strictly aquatic macroinvertebrate taxa. Ecology and Evolution 12: e8807.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Jūratė Lesutienė and Gintautas Vaitonis for help during the fieldwork in Ukraine in 2012. This study was supported by the Research Council of Lithuania (Contract No. S-MIP-20-26). Sampling in Ukraine in 2012 was supported by a grant from the Research Council of Lithuania (Contract No. LEK-10/2012). HM was supported by the ALLEA “European Funds for Displaced Scientists” (EFDS) (Contract No. EFDS-FL1-27).

Funding

This study was funded by the Research Council of Lithuania (Contract No. S-MIP-20-26). Sampling in Ukraine in 2012 was supported by a grant from the Research Council of Lithuania (Contract No. LEK-10/2012). HM was supported by the ALLEA “European Funds for Displaced Scientists” (EFDS) (Contract No. EFDS-FL1-27).

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Authors and Affiliations

  1. Laboratory of Evolutionary Ecology of Hydrobionts, Nature Research Centre, Vilnius, Lithuania

    Denis Copilaş-Ciocianu, Eglė Šidagytė-Copilas & Kęstutis Arbačiauskas

  2. Department of Water Quality, Institute of Marine Biology of National Academy of Sciences of Ukraine, Odesa, Ukraine

    Mikhail O. Son & Halyna Morhun

  3. Department of Invertebrate Zoology and Hydrobiology, University of Lodz, Lodz, Poland

    Halyna Morhun

  4. Naturalis Biodiversity Center, Leiden, The Netherlands

    Jan Niklas Macher

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  1. Denis Copilaş-Ciocianu
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  2. Eglė Šidagytė-Copilas
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  3. Mikhail O. Son
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  4. Halyna Morhun
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  5. Jan Niklas Macher
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  6. Kęstutis Arbačiauskas
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Correspondence to Denis Copilaş-Ciocianu.

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Predictions and residuals of the LMEMs for the COI (top) and OPS (bottom) marker diversity metrics (see Table 3 for model effects tests). Metric abbreviations: Hn – haplotype number, Hd – haplotype diversity, Pi – nucleotide diversity, K – average number of nucleotide differences. Thick lines represent estimated means. Significant multiple comparisons are indicated by thin connecting lines of different patterns, absence indicating results with P > 0.05

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List of sampling localities and associated information is provided in Table S1

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Copilaş-Ciocianu, D., Šidagytė-Copilas, E., Son, M.O. et al. Genetic diversity of Ponto-Caspian amphipods throughout the invaded Baltic and native NW Black Sea donor ranges: does introduction mode matter?. Hydrobiologia 850, 3061–3076 (2023). https://doi.org/10.1007/s10750-023-05230-6

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