Temporal Dynamics of Biological Invasions: Perception of Host Quality Differs Between Native and Alien Host Species

. 2025 Oct ; 15 (10) : e72270. [epub] 20251006

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid41059356

The spread of non-native species into new regions is a dynamic process driven by behavioural adaptations to local environments and species interactions. Interactions between coexisting populations can lead to localised coevolutionary patterns, shaped by the duration of their co-occurrence. We investigated the relationship between the European bitterling fish (Rhodeus amarus), a parasitic fish that lays eggs in the gills of unionid mussels, and an invasive mussel host, Sinanodonta woodiana, which has spread across Europe over the past 50 years. The bitterling, a host generalist, can parasitise any European unionid mussel species, but its reproductive success with S. woodiana is limited due to the mussel's ability to reject bitterling eggs. We tested three hypotheses on the role of rapid local coevolution in host choice using S. woodiana populations with recent (5 years), intermediate (17 years), and long-term (40+ years) associations with European bitterling. We experimentally evaluated the spawning preferences of four bitterling populations: three coexisting with their respective S. woodiana populations and one naïve to S. woodiana. All bitterling populations avoided S. woodiana from the most recently established population. Neither local coexistence nor individual mussel quality influenced bitterling responses to S. woodiana. In contrast, bitterling selected native Anodonta anatina mussels based on individual quality rather than population identity. These findings suggest that native species can recognise and avoid an invasive host at the invasion front, where co-occurrence is recent.

Zobrazit více v PubMed

Aldridge, D. C. 1999. “Development of European Bitterling in the Gills of Freshwater Mussels.” Journal of Fish Biology 54: 138–151.

Anil, A. N. , Mehdi I., Douda K., Smith C., and Reichard M.. 2024. “Reciprocal Transplant Experiments Demonstrate a Dynamic Coevolutionary Relationship Between Parasitic Mussel Larvae and Bitterling Fishes.” Freshwater Biology 69: 1525–1536.

Bartáková, V. , Bryja J., Reichard M., Bartáková V., Bryja J., and Reichard M.. 2018. “Fine‐Scale Genetic Structure of the European Bitterling at the Intersection of Three Major European Watersheds.” BMC Evolutionary Biology 18: 1–15. PubMed PMC

Bartáková, V. , Bryja J., Šanda R., et al. 2019. “High Cryptic Diversity of Bitterling Fish in the Southern West Palearctic.” Molecular Phylogenetics and Evolution 133: 1–11. PubMed

Benkő‐Kiss, Á. , Ferincz Á., Kováts N., and Paulovits G.. 2013. “Spread and Distribution Pattern of

Berenbaum, M. R. , Zangerl A. R., Berenbaum M. R., and Zangerl A. R.. 1998. “Chemical Phenotype Matching Between a Plant and Its Insect Herbivore.” Proceedings of the National Academy of Sciences of the United States of America 95: 13743–13748. PubMed PMC

Bevins, S. N. 2019. “Parasitism, Host Behavior, and Invasive Species.” In Encyclopedia of Animal Behavior, edited by Choe J. C., 2nd ed. Elsevier, Academic Press.

Bonat, W. H. , Jørgensen B., Kokonendji C. C., Hinde J., and Demétrio C. G. B.. 2018. “Extended Poisson–Tweedie: Properties and Regression Models for Count Data.” Statistical Modelling 18: 24–49.

Bourchier, R. , Hansen R., Lym R., et al. 2006. Biology and Biological Control of Leafy Spurge. Forest Health Technology Enterprise Team. U.S. Department of Agriculture.

Bryja, J. , Smith C., Konečný A., and Reichard M.. 2010. “Range‐Wide Population Genetic Structure of the European Bitterling ( PubMed

Callaway, R. M. , and Ridenour W. M.. 2004. “Novel Weapons: Invasive Success and the Evolution of Increased Competitive Ability.” Frontiers in Ecology and the Environment 2: 436–443.

Colautti, R. I. , Ricciardi A., Grigorovich I. A., and MacIsaac H. J.. 2004. “Is Invasion Success Explained by the Enemy Release Hypothesis?” Ecology Letters 7: 721–733.

Cox, J. G. , and Lima S. L.. 2006. “Naiveté and an Aquatic–Terrestrial Dichotomy in the Effects of Introduced Predators.” Trends in Ecology & Evolution 21: 674–680. PubMed

Crooks, J. A. 2005. “Lag Times and Exotic Species: The Ecology and Management of Biological Invasions in Slow‐motion1.” Écoscience 12: 316–329.

David, P. , Thébault E., Anneville O., Duyck P.‐F., Chapuis E., and Loeuille N.. 2017. “Impacts of Invasive Species on Food Webs: A Review of Empirical Data.” Networks of Invasion: A Synthesis of Concepts 56: 1–60.

Deng, B. , Riccardi N., Urbańska M., Marjomäki T. J., Andrzejewski W., and Taskinen J.. 2024. “Lower Parasite Pressure in Invasive Freshwater Bivalves Than in Sympatric Native Unionidae Mussels in Southern European Lakes.” Biological Invasions 27: 10.

Douda, K. , Zieritz A., Vodáková B., et al. 2024. “Review of the Globally Invasive Freshwater Mussels in the Genus

Gallien, L. , and Carboni M.. 2017. “The Community Ecology of Invasive Species: Where Are We and What's Next?” Ecography 40: 335–352.

Gendron, A. D. , Marcogliese D. J., and Thomas M.. 2011. “Invasive Species Are Less Parasitized Than Native Competitors, but for How Long? The Case of the Round Goby in the Great Lakes‐St. Lawrence Basin.” Biological Invasions 14: 367–384.

Halabowski, D. , Pyrzanowski K., Zięba G., et al. 2025. “The Impact of Invasive PubMed PMC

Halabowski, D. , Reichard M., Pyrzanowski K., et al. 2024. “The Depressed River Mussel

Hartig, F. 2021. “DHARMa: Residual Diagnostics for Hierarchical (Multi‐Level / Mixed) Regression Models. 0.4.7.”

Hobbs, R. J. , Arico S., Aronson J., et al. 2006. “Novel Ecosystems: Theoretical and Management Aspects of the New Ecological World Order.” Global Ecology and Biogeography 15: 1–7.

Holčík, J. , and Wit J. J. D. D.. 1962. “The Taxonomic Characteristics of Hybrid

Hulme, P. E. 2007. “Biological Invasions in Europe: Drivers, Pressures, States, Impacts and Responses.” In Biodiversity Under Threat, edited by Hester R. H. R. M.. University Press.

Keane, R. M. , and Crawley M. J.. 2002. “Exotic Plant Invasions and the Enemy Release Hypothesis.” Trends in Ecology & Evolution 17: 164–170.

Kitamura, J. , Nagata N., Nakajima J., and Sota T.. 2012. “Divergence of Ovipositor Length and Egg Shape in a Brood Parasitic Bitterling Fish Through the Use of Different Mussel Hosts.” Journal of Evolutionary Biology 25: 566–573. PubMed

Kolar, C. S. , and Lodge D. M.. 2001. “Progress in Invasion Biology: Predicting Invaders.” Trends in Ecology & Evolution 16: 199–204. PubMed

Konečný, A. , Popa O. P., Bartáková V., et al. 2018. “Modelling the Invasion History of PubMed PMC

Labecka, A. M. , and Reichard M.. 2025. “The Reproductive Costs of Bitterling Fish and Zebra Mussel Parasitism to a Unionid Mussel.” Aquaculture 595: 741515.

Laland, K. N. 2015. “On Evolutionary Causes and Evolutionary Processes.” Behavioural Processes 117: 97–104. PubMed

Lankau, R. A. , Nuzzo V., Spyreas G., and Davis A. S.. 2009. “Evolutionary Limits Ameliorate the Negative Impact of an Invasive Plant.” Proceedings of the National Academy of Sciences of the United States of America 106: 15362–15367. PubMed PMC

Leger, E. A. , and Espeland E. K.. 2010. “Coevolution Between Native and Invasive Plant Competitors: Implications for Invasive Species Management.” Evolutionary Applications 3: 169–178. PubMed PMC

Levine, J. M. , and D'Antonio C. M.. 1999. “Elton Revisited: A Review of Evidence Linking Diversity and Invasibility.” Oikos 87: 15–26.

Lockwood, J. L. , Cassey P., and Blackburn T.. 2005. “The Role of Propagule Pressure in Explaining Species Invasions.” Trends in Ecology & Evolution 20: 223–228. PubMed

Lymbery, A. J. , Morine M., Kanani H. G., Beatty S. J., and Morgan D. L.. 2014. “Co‐Invaders: The Effects of Alien Parasites on Native Hosts.” International Journal for Parasitology: Parasites and Wildlife 3: 171–177. PubMed PMC

Marčić, Z. , Prenz P., Horvatić S., et al. 2024. “Is Bitterling (

Mehler, K. , Labecka A. M., Sîrbu I., Flores N. Y., Leuven R. S. E. W., and Collas F. P. L.. 2024. “Recent and Future Distribution of the Alien Chinese Pond Mussel

Mills, S. C. , and Reynolds J. D.. 2002a. “Host Species Preferences by Bitterling,

Mills, S. C. , and Reynolds J. D.. 2002b. “Mussel Ventilation Rates as a Proximate Cue for Host Selection by Bitterling, PubMed

Mills, S. C. , and Reynolds J. D.. 2004. “The Importance of Species Interactions in Conservation: The Endangered European Bitterling

Mills, S. C. , Taylor M. I., and Reynolds J. D.. 2005. “Benefits and Costs to Mussels From Ejecting Bitterling Embryos: A Test of the Evolutionary Equilibrium Hypothesis.” Animal Behaviour 70: 31–37.

Mooney, H. A. , and Cleland E. E.. 2001. “The Evolutionary Impact of Invasive Species.” Proceedings of the National Academy of Sciences of the United States of America 98: 5446–5451. PubMed PMC

Moran, E. V. , and Alexander J. M.. 2014. “Evolutionary Responses to Global Change: Lessons From Invasive Species.” Ecology Letters 17: 637–649. PubMed

Paunović, M. , Csányi B., Simić V., Stojanovic B., and Cakic P.. 2006. “Distribution of

Pearson, D. E. , Ortega Y. K., Eren Ö., and Hierro J. L.. 2018. “Community Assembly Theory as a Framework for Biological Invasions.” Trends in Ecology & Evolution 33: 313–325. PubMed

Pfeiffer, M. , Mildner M., Günter C. P., and Leschner M.. 2025. “The Asian Clam

Phillips, B. L. , Brown G. P., Webb J. K., and Shine R.. 2006. “Invasion and the Evolution of Speed in Toads.” Nature 439: 803. PubMed

Phillips, B. L. , and Shine R.. 2005. “The Morphology, and Hence Impact, of an Invasive Species (The Cane Toad,

Phillips, B. L. , and Shine R.. 2006. “An Invasive Species Induces Rapid Adaptive Change in a Native Predator: Cane Toads and Black Snakes in Australia.” Proceedings of the Royal Society B: Biological Sciences 273: 1545–1550. PubMed PMC

Reichard, M. , Douda K., Przybylski M., et al. 2015. “Population‐Specific Responses to an Invasive Species.” Proceedings of the Royal Society B: Biological Sciences 282: 1063. PubMed PMC

Reichard, M. , Liu H., and Smith C.. 2007. “The Co‐Evolutionary Relationship Between Bitterling Fishes and Freshwater Mussels: Insights From Interspecific Comparisons.” Evolutionary Ecology Research 9: 239–259.

Reichard, M. , Ondracková M., Przybylski M., Liu H., and Smith C.. 2006. “The Costs and Benefits in an Unusual Symbiosis: Experimental Evidence That Bitterling Fish ( PubMed

Reichard, M. , Polačik M., Tarkan A. S., et al. 2010. “The Bitterling‐Mussel Coevolutionary Relationship in Areas of Recent and Ancient Sympatry.” Evolution 64: 3047–3056. PubMed

Reichard, M. , Przybylski M., Kaniewska P., Liu H., and Smith C.. 2007. “A Possible Evolutionary Lag in the Relationship Between Freshwater Mussels and European Bitterling.” Journal of Fish Biology 70: 709–725.

Reichard, M. , Vrtílek M., Douda K., and Smith C.. 2012. “An Invasive Species Reverses the Roles in a Host–Parasite Relationship Between Bitterling Fish and Unionid Mussels.” Biology Letters 8: 601–604. PubMed PMC

Rouchet, R. , Smith C., Liu H., et al. 2017. “Avoidance of Host Resistance in the Oviposition‐Site Preferences of Rose Bitterling.” Evolutionary Ecology 31: 769–783.

Roznik, E. A. , Surbaugh K. L., Cano N., and Rohr J. R.. 2020. “Elucidating Mechanisms of Invasion Success: Effects of Parasite Removal on Growth and Survival Rates of Invasive and Native Frogs.” Journal of Applied Ecology 57: 1078–1088. PubMed PMC

Sage, R. F. 2020. “Global Change Biology: A Primer.” Global Change Biology 26: 3–30. PubMed

Saul, W.‐C. , and Jeschke J. M.. 2015. “Eco‐Evolutionary Experience in Novel Species Interactions.” Ecology Letters 18: 236–245. PubMed

Shine, R. 2012. “Invasive Species as Drivers of Evolutionary Change: Cane Toads in Tropical Australia.” Evolutionary Applications 5: 107–116. PubMed PMC

Simberloff, D. , Martin J.‐L., Genovesi P., et al. 2013. “Impacts of Biological Invasions: What's What and the Way Forward.” Trends in Ecology & Evolution 28: 58–66. PubMed

Smith, C. , Douglas A., and Jurajda P.. 2002. “Sexual Conflict, Sexual Selection and Sperm Competition in the Spawning Decisions of Bitterling,

Smith, C. , Reichard M., Jurajda P., and Przybylski M.. 2004. “The Reproductive Ecology of the European Bitterling (

Smith, C. , Rippon K., Douglas A., and Jurajda P.. 2001. “A Proximate Cue for Oviposition Site Choice in the Bitterling (

Smith, C. , Warren M., Rouchet R., and Reichard M.. 2014. “The Function of Multiple Ejaculations in Bitterling.” Journal of Evolutionary Biology 27: 1819–1829. PubMed

Spence, R. , Reichard M., and Smith C.. 2013. “Strategic Sperm Allocation and a Coolidge Effect in an Externally Fertilizing Species.” Behavioral Ecology 24: 82–88.

Stewart, P. S. , Hill R. A., Stephens P. A., Whittingham M. J., and Dawson W.. 2021. “Impacts of Invasive Plants on Animal Behaviour.” Ecology Letters 24: 891–907. PubMed

Strauss, S. Y. , Lau J. A., and Carroll S. P.. 2006. “Evolutionary Responses of Natives to Introduced Species: What Do Introductions Tell Us About Natural Communities?” Ecology Letters 9: 357–374. PubMed

Strayer, D. L. , Eviner V. T., Jeschke J. M., and Pace M. L.. 2006. “Understanding the Long‐Term Effects of Species Invasions.” Trends in Ecology & Evolution 21: 645–651. PubMed

Stuart, Y. E. , Campbell T. S., Hohenlohe P. A., Reynolds R. G., Revell L. J., and Losos J. B.. 2014. “Rapid Evolution of a Native Species Following Invasion by a Congener.” Science 346: 463–466. PubMed

Taraschewski, H. 2006. “Hosts and Parasites as Aliens.” Journal of Helminthology 80: 99–128. PubMed

Thompson, J. N. 1994. The Coevolutionary Process. University of Chicago press.

Thompson, J. N. 2010. “Four Central Points About Coevolution.” Evolution: Education and Outreach 3: 7–13.

Torchin, M. E. , Lafferty K. D., Dobson A. P., McKenzie V. J., and Kuris A. M.. 2003. “Introduced Species and Their Missing Parasites.” Nature 421: 628–630. PubMed

Torchin, M. E. , Lafferty K. D., and Kuris A. M.. 2001. “Release From Parasites as Natural Enemies: Increased Performance of a Globally Introduced Marine Crab.” Biological Invasions 3: 333–345.

Traveset, A. , and Richardson D. M.. 2006. “Biological Invasions as Disruptors of Plant Reproductive Mutualisms.” Trends in Ecology & Evolution 21: 208–216. PubMed

U.S. Fish & Wildlife Service . 2019. Ecological Risk Screening Summary—Bitterling (Rhodeus sericeus). U.S. Fish & Wildlife Service.

Vilà, M. , Basnou C., Pyšek P., et al. 2009. “How Well Do We Understand the Impacts of Alien Species on Ecosystem Services? A Pan‐European, Cross‐Taxa Assessment.” Frontiers in Ecology and the Environment 8: 135–144.

Whitney, K. D. , and Gabler C. A.. 2008. “Rapid Evolution in Introduced Species, ‘Invasive Traits’ and Recipient Communities: Challenges for Predicting Invasive Potential.” Diversity and Distributions 14: 569–580.

Yi, W. , Reichard M., Rücklin M., and Richardson M. K.. 2024. “Parasitic Fish Embryos Do a “Front‐Flip” on the Yolk to Resist Expulsion From the Host.” Proceedings of the National Academy of Sciences 121: e2310082121. PubMed PMC

Zangerl, A. R. , and Berenbaum M. R.. 2003. “Phenotype Matching in Wild Parsnip and Parsnip Webworms: Causes and Consequences.” Evolution 57: 806–815. PubMed

Zdanowski, B. 1996. Nieznana szczeżuja (Anodonta sp.) w podgrzanych Jeziorach Konińskich. XII‐th Krajowe Seminarium Malakologiczne.

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.28644491

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...