The role of local adaptation in shaping fish‐mussel coevolution

Abstract

Abstract1. The survival of affiliate (dependent) species in a changing environment is determined by the interactions between the affiliate species and their available hosts.However, the patterns of spatial and temporal changes in host compatibility are often unknown despite host shifts having direct impact on the persistence of local populations. Bivalves of the order Unionida (freshwater mussels) are a functionally important but declining group of affiliate species, which are dependent on freshwater fish to host their parasitic larvae. The role of local adaptations and host fish resistance in shaping freshwater mussel host relationships remains poorly understood. 2.We used an invasive East Asian unionid bivalve, Sinanodonta woodiana, and its potential host fishes to study the mechanisms shaping fish-mussel coevolution using a combination of laboratory cross-exposure methods and field-collected data. We tested whether generalist host use of S. woodiana is pertinent to native host species, with special attention to bitterling fishes (Cyprinidae: Acheilognathinae) that are characterised by a mutual association with freshwater mussels. We also tested whether the pattern of the parasite-host association varies temporally (between areas of ancient and recent sympatry) and spatially (at a sub-basin level in its native range). 3.Results revealed the ability of S. woodiana to widely exploit non-bitterling host fishes at a global scale. In contrast, the ability of S. woodiana to exploit closely associated bitterling fishes was low in its native range (with ancient sympatry). In areas of recent sympatry (non-native S. woodiana range in Europe), S. woodiana glochidia were demonstrated to readily parasitise local, evolutionarily naive bitterling species at high density. 4.The results of a population-level experiment with three native populations of S. woodiana and rose bitterling, Rhodeus ocellatus, from various sub-basins of the River Yangtze confirmed that mussel populations vary in their compatibility with particular host populations. However, there was no evidence of population-specific adaptive coevolution.5. This study provides the first evidence for a role of fish counter-adaptations against freshwater mussel glochidia, and documents the importance of population-level variation in shaping compatibility between glochidia and their host

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

“…That period is sufficient for successful long‐distance dispersal associated with the trade in freshwater fishes for aquaculture and angling purposes across Europe (Litvak & Mandrak, ). While many unionid mussel species are host specialists (Modesto et al., ), S. woodiana has an extremely extensive host range and can utilize all European freshwater fish species hitherto tested (Douda et al., , ). This feature is not unique to invasive S. woodiana populations, because S. woodiana also utilizes an exceptionally broad range of host species in its native range (Douda et al., ; Dudgeon & Morton, ).…”

“…While many unionid mussel species are host specialists (Modesto et al., ), S. woodiana has an extremely extensive host range and can utilize all European freshwater fish species hitherto tested (Douda et al., , ). This feature is not unique to invasive S. woodiana populations, because S. woodiana also utilizes an exceptionally broad range of host species in its native range (Douda et al., ; Dudgeon & Morton, ). This trait is a highly effective preadaptation for rapid and successful invasion (Torchin & Mitchell, ).…”

Silent invasion: Sinanodonta woodiana successfully reproduces and possibly endangers native mussels in the north of its invasive range in Europe

“…The competitive advantage of S. woodiana over native mussels can be predicted from a number of features in its reproductive biology. It reaches sexual maturity already in the first year of life at the shell length of approximately 30 mm (Dudgeon & Morton, 1983;Labecka & Domagala, 2018), whereas native Anodontinae reach maturity at 2 years or later (Zieritz & Aldridge, 2011), it produces a significantly larger number of eggs per female (Wächtler et al, 2001), is capable of continuous reproduction throughout the year (Labecka & Domagala, 2018), and contrary to many native mussels which are host specialists (Modesto et al, 2018), it can utilize an extremely broad range of fish hosts to complete its development (Douda et al, 2012;Douda, Liu, et al, 2017). Additionally, S. woodiana induces strong cross-resistance in parasitized fish (Donrovich et al, 2017).…”

“…Factors contributing to its invasion include broad tolerance with regard to habitat (Lajtner & Crnčan, ), food (Liu, Hao, Iseri, Kuba, & Zhang, ), and pollution (Bielen et al, ; Corsi et al, ). Importantly, it is a host generalist not limited in its spread by the availability of co‐invasive fish (Douda, Liu, et al, ; Douda, Vrtílek, Slavík, & Reichard, ; Hua, Xu, & Wen, ).…”

An unexpected host for the endangered giant freshwater pearl mussel Margaritifera auricularia (Spengler, 1793) as a conservation tool

“…Previous studies have suggested that invasive fish species are less suitable as hosts for freshwater mussels than native ones, probably owing to a co-evolutionary mechanism of host compatibility between mussels and host fish species (Douda et al, 2013;Salonen, Marjomäki, & Taskinen, 2016;Taeubert, Gum, & Geist, 2012). According to the available data, the vast majority of freshwater mussel species use only native hosts, whereas the glochidia of only a few host generalist species have been shown to metamorphose successfully on non-native fishes (Douda et al, 2017;Huber & Geist, 2017;Modesto et al, 2018;Teixeira et al, 2018).…”