An invasive species reverses the roles in a host–parasite relationship between bitterling fish and unionid mussels

Abstract

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.

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

“…While populations from Central Poland were used by R. amarus for oviposition, with all bitterling embryos later ejected, S. woodiana populations from the southern Czech Republic were completely avoided by R. amarus , thereby mitigating the costs of failed development. Hence, the identity of S. woodiana populations determines the impact of S. woodiana on native R. amarus , from almost neutral to highly negative (Reichard, Vrtílek, Douda, & Smith, ; Reichard et al., ). The current study demonstrated that the two S. woodiana populations previously used to test their response to bitterling fish are genetically differentiated (PLLI and CZKY populations, respectively).…”

Molecular cloning, characterization, and the response of Cu/Zn superoxide dismutase and catalase to PBDE-47 and -209 from the freshwater bivalve Anodonta woodiana

“…Bivalve molluscs are ubiquitous, sedentary filter feeders, which can bio-accumulate pollutants to a high degree [16,17]. The Chinese pond mussel (the Eastern Asiatic freshwater clam or swanmussel), bivalve Anodonta woodiana functions as a main criteria required for a bio-indicator organism [18,19]. Earlier studies have revealed the ability of Sinanodonta woodiana to accumulate trace elements and pesticides [20,21], as well as its potential to detect genotoxicity [22].…”

Phylogenetic relationships of Acheilognathidae (Cypriniformes: Cyprinoidea) as revealed from evidence of both nuclear and mitochondrial gene sequence variation: Evidence for necessary taxonomic revision in the family and the identification of cryptic species

“…Fertilization occurs in the mussel gill cavity and development is completed in the host mussel gill chamber (Smith et al, 2004). This breeding association makes species of bitterlings a focus of research aimed at understanding coevolutionary dynamics, life-history evolution, sexual selection, sperm competition, development and mate choice (Agbali et al, 2011;Casalini et al, 2009;Kitamura et al, 2012;Mills et al, 2005;Reichard et al, 2006Reichard et al, , 2007Reichard et al, , 2012; .…”