The impact of multiple invading species can be magnified owing to mutual facilitation--termed 'invasional meltdown'--but invasive species can also be adversely affected by their interactions with other invaders. Using a unique reciprocal host-parasite relationship between a bitterling fish (Rhodeus amarus) and unionid mussels, we show that an invasive mussel reverses the roles in the relationship. Bitterling lay their eggs into mussel gills, and mussel larvae parasitize fish. Bitterling recently colonized Europe and parasitize all sympatric European mussels, but are unable to use a recently invasive mussel, Anodonta woodiana. The parasitic larvae of A. woodiana successfully develop on R. amarus, whereas larvae of European mussels are rejected by bitterling. This demonstrates that invading species may temporarily benefit from a coevolutionary lag by exploiting evolutionarily naive hosts, but the resulting relaxed selection may facilitate its exploitation by subsequent invading species, leading to unexpected consequences for established interspecific relationships.

Academy of Sciences of Czech Republic Institute of Vertebrate Biology Květná 8 60365 Brno Czech Republic

Zobrazit více v PubMed

Simberloff D., Von Holle M. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biol. Inv. 1, 21–3210.1023/A:1010086329619 (doi:10.1023/A:1010086329619) DOI

Kiers E. T., Palmer T. M., Ives A. R., Bruno J. F., Bronstein J. L. 2010. Mutualisms in a changing world: an evolutionary perspective. Ecol. Lett. 13, 1459–147410.1111/j.1461-0248.2010.01538.x (doi:10.1111/j.1461-0248.2010.01538.x) PubMed DOI

Thompson J. N., Cunningham B. C. 2002. Geographic structure and dynamics of coevolutionary selection. Nature 417, 735–73810.1038/nature00810 (doi:10.1038/nature00810) PubMed DOI

Jahner J. P., Bonilla M. M., Badik K. J., Shapiro A. M., Forister M. L. 2011. Use of exotic hosts by Lepidoptera: widespread species colonize more novel hosts. Evolution 65, 2719–272410.1111/j.1558-5646.2011.01310.x (doi:10.1111/j.1558-5646.2011.01310.x) PubMed DOI

Chew F. S. 1977. Coevolution of pierid butterflies and their cruciferous foodplants. II. The distribution of eggs on potential foodplants. Evolution 31, 568–57910.2307/2407522 (doi:10.2307/2407522) PubMed DOI

Reichard M., Ondračková M., Przybylski M., Liu H., Smith C. 2006. The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J. Evol. Biol. 19, 788–79610.1111/j.1420-9101.2005.01051.x (doi:10.1111/j.1420-9101.2005.01051.x) PubMed DOI

Smith C., Reichard M., Jurajda P., Przybylski M. 2004. The reproductive ecology of the European bitterling (Rhodeus sericeus). J. Zool. 262, 107–12410.1017/S0952836903004497 (doi:10.1017/S0952836903004497) DOI

Van Damme D., Bogutskaya N., Hoffmann R., Smith C. 2007. The introduction of the European bitterling Rhodeus amarus to west and central Europe. Fish Fisher. 8, 79–10610.1111/j.1467-2679.2007.00239.x (doi:10.1111/j.1467-2679.2007.00239.x) DOI

Bryja J., Smith C., Konečný A., Reichard M. 2010. Range-wide population genetic structure of the European bitterling (Rhodeus amarus) based on microsatellite and mitochondrial DNA analysis. Mol. Ecol. 19, 4708–472210.1111/j.1365-294X.2010.04844.x (doi:10.1111/j.1365-294X.2010.04844.x) PubMed DOI

Reichard M., Polačik M., Tarkan A. S., Spence R., Gaygusuz O., Ercan E., Ondračková M., Smith C. 2010. The bitterling mussel coevolutionary relationship in areas of recent and ancient sympatry. Evolution 64, 3047–305610.1111/j.1558-5646.2010.01032.x (doi:10.1111/j.1558-5646.2010.01032.x) PubMed DOI

Rogers-Lowery C. L., Dimock R. V., Jr, Kuhn R. E. 2007. Antibody response of bluegill sunfish during development of acquired resistance against the larvae of the freshwater mussel Utterbackia imbecillis. Dev. Comp. Immunol. 31, 143–15510.1016/j.dci.2006.05.011 (doi:10.1016/j.dci.2006.05.011) PubMed DOI

Bauer G., Wächtler K. 2001. Ecology and evolution of the freshwater mussels unionoida. Berlin, Germany: Springer

Reichard M., Liu H., Smith C. 2007. The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol. Ecol. Res. 9, 239–259

Watters G. T. 1997. A synthesis and review of the expanding range of the Asian freshwater mussel Anodonta woodiana (Lea, 1834) (Bivalvia: Unionidae). Veliger 40, 152–156

Kondo T., Yamashita J., Kano M. 1984. Breeding ecology of five species of bitterling (Pisces: Cyprinidae) in a small creek. Physiol. Ecol. Jpn. 21, 53–62

Reichard M., Przybylski M., Kaniewska P., Liu H., Smith C. 2007. A possible evolutionary lag in the relationship between freshwater mussels and European bitterling. J. Fish Biol. 70, 709–72510.1111/j.1095-8649.2007.01333.x (doi:10.1111/j.1095-8649.2007.01333.x) DOI

Kottelat M., Freyhof J. 2007. Handbook of European freshwater fishes. Cornol, Switzerland: Kottelat

Bohlen J., Šlechtová V., Bogutskaya N., Freyhof J. 2006. Across Siberia and over Europe: phylogenetic relationships of the freshwater fish genus Rhodeus in Europe and the phylogenetic position of R. sericeus from the River Amur. Mol. Phyl. Evol. 40, 856–86510.1016/j.ympev.2006.04.020 (doi:10.1016/j.ympev.2006.04.020) PubMed DOI

Lahti D. C. 2005. Evolution of bird eggs in the absence of cuckoo parasitism. Proc. Natl Acad. Sci. USA 102, 18 057–18 06210.1073/pnas.0508930102 (doi:10.1073/pnas.0508930102) PubMed DOI PMC

Rothstein S. I. 1990. A model system for coevolution: avian brood parasitism. Annu. Rev. Ecol. Syst. 21, 481–50810.1146/annurev.es.21.110190.002405 (doi:10.1146/annurev.es.21.110190.002405) DOI

Cianfanelli S., Lori E., Bodon M. 2007. Non-indigenous freshwater molluscs and their distribution in Italy. In Biological invaders in inland waters: profiles, distribution, and threats (ed. Gherardi F.), pp. 103–121 Berlin, Germany: Springer

The impact of invasive Sinanodonta woodiana (Bivalvia, Unionidae) and mussel macroparasites on the egg distribution of parasitic bitterling fish in host mussels

Individual copy number variation and extensive diversity between major MHC-DAB1 allelic lineages in the European bitterling

Intensity-dependent energetic costs in a reciprocal parasitic relationship

Modelling the invasion history of Sinanodonta woodiana in Europe: Tracking the routes of a sedentary aquatic invader with mobile parasitic larvae

Bayesian inference supports the host selection hypothesis in explaining adaptive host specificity by European bitterling

Population-specific responses to an invasive species