ALBERT

Description: Invasive species, and especially invasive parasites, represent excellent models to study ecological and evolutionary mechanisms in the wild. To understand these processes, it is crucial to obtain more knowledge on the native range, invasion routes and invasion history of invasive parasites. We investigated the consecutive invasions of two parasitic copepods (Mytilicola intestinalis and Mytilicola orientalis) by combining an extensive literature survey covering the reported putative native regions and the present-day invaded regions with a global phylogeography of both species. The population genetic analyses based on partial COI sequences revealed significant population differentiation for M. orientalis within the native region in Japan, while introduced populations in North America and Europe could not be distinguished from the native ones. Thus, M. orientalis’ invasion history resembles the genetic structure and recent spread of its principal host, the Pacific oyster, Crassostrea gigas, while M. intestinalis lacks population genetic structure and has an overall low genetic diversity. Therefore, the native origin of M. intestinalis remains unclear. With this study, we demonstrate that even highly related and biologically similar invasive species can differ in their invasion genetics. From this, we conclude that extrapolating invasion genetics dynamics from related invasive taxa may not always be possible.

Description: Biological invasions of parasites offer ideal opportunities to study coevolution in nature - especially when hosts are faced with repeated invasions of parasites. Such coinvasions not only lead to selection on the host but also to selection on parasites arising from direct competition. Here, we present data from a crossed coinfection experiment using two closely related copepod parasites that have invaded the Eastern Atlantic, infecting mussels. One is the specialist Mytilicola intestinalis, that invaded from the Mediterranean Sea in the 1930s and the other one is the generalist Mytilicola orientalis that invaded from Japan in the 1990ies. This system thus offers the opportunity to study host-parasite interactions along a gradient of different coevolutionary timescales and host specificity. Here we report the first results of this experiment on the phenotypic level focussing on the balance and trade-offs between host and parasite traits, i.e. infectivity - virulence for the parasites and virulence-tolerance for the hosts. We find different interactions along these trade-offs between both interactions. We also find that the generalist invader is outcompeting the old invader.

Description: Parasites are ubiquitous in nature and the strong natural selection pressures they impose on their hosts are predicted to elicit rapid evolutionary adaptive responses of hosts towards their parasites, leading to antagonistic host–parasite co-evolution. While most of what we know about these processes stems from laboratory studies with a restricted set of model organisms, much less is known about host–parasite co- evolution in the wild, largely due to logistical challenges of experimental manipulations on an ecosystem scale. Biological invasions represent excellent opportunities to overcome these logistical issues and study host–parasite interactions and co-evolution in non-model species in the wild, as they can be seen as “natural experiments” in which different invasion scenarios lead to different ecological and evolutionary dynamics. This dissertation utilises the invasions of two parasitic copepods Mytilicola intestinalis and Mytilicola orientalis in the Wadden Sea to address the study of host–parasite co-evolution and co-infection in non-model species in the wild. This conceptual approach and the biological system are introduced in Chapter 1. Validation of the presumed origins and invasion routes of both parasites were still lacking, therefore my first aim was to confirm them. This was done through an extensive literature review, in combination with invasion genetics (Chapter 2), which resulted in the validation of Japan as the native and North America and Europe as the invaded ranges of M. orientalis (where it was co-introduced with the Pacific oyster Magallana gigas), while it remained unclear whether the Mediterranean Sea is really the native range of M. intestinalis. The biological invasion of M. intestinalis and later M. orientalis created a situation in which two congeneric species co-occur and share the same novel host in their invaded range. The two parasites have different degrees of host specificity in the Wadden Sea, as M. intestinalis only infects blue mussels Mytilus edulis, while M. orientalis also infects Pacific oysters M. gigas, and at least two other bivalve species. As generalists and specialists are not expected to occupy the same niche over extended periods of time, my second aim was to investigate potential competitive interactions between the two parasites. In an experiment, I showed that Pacific oysters are not suitable hosts for M. intestinalis (Chapter 3). Furthermore, from an infection experiment with mussels, there were no indications of direct competition or superiority of either parasite in co-infections, but the infection rate of M. orientalis was lower than that of M. intestinalis (Chapter 3). Therefore, the ongoing invasion of M. orientalis in the Northern Wadden Sea at locations where M. intestinalis is already present is more likely to be facilitated by the other hosts M. orientalis can utilise, than by competitive interactions within the shared host. Moreover, I highlighted the use of biological invasions of parasites to study host–parasite co-evolution in non-model organisms in the wild. By making experimental cross-infections of mussels and M. intestinalis from two invasion fronts with similar co-evolutionary time periods (Texel and Sylt) and an uninvaded location (Kiel), I could study evolutionary changes after introduction. Kiel mussels lacked a co-evolved response to parasite infection. Furthermore, invasions of M. intestinalis at separate fronts in the Wadden Sea led to different evolutionary trajectories in both hosts and parasites in the mussel–M. intestinalis system, with pre-infection traits (infectivity/resistance) evolving on Texel, while post-infection traits (virulence/tolerance) may have evolved on Sylt (Chapter 4). A dual-species transcriptomics approach on Texel and Sylt hosts and parasites of the sympatric, allopatric and control treatments was used next to document the molecular underpinnings of the different evolutionary trajectories. This uncovered a general immune response of mussels towards M. intestinalis infections, as well as several candidate genes and processes that mediate the different evolutionary trajectories (Chapter 5). The combination of studying responses on the phenotypic level and the transcriptional level through dual transcriptomics thus promises to be a fruitful approach to unravel the molecular mechanisms behind evolution of host–parasite interactions in many other non-model organisms. In general, this dissertation demonstrates the value of using biological invasions to investigate host–parasite co-evolution in the wild, which is especially promising for research on non-model organisms. Future research should, however, further unravel the relative importance of phenotypic plasticity and genetic determinism for the co- evolutionary dynamics between hosts and parasites, but should also investigate the potential effects of other factors, such as, in the case of Mytilicola, the roles of the mussel microbiome and the hyperparasite Unikaryon mytilicolae (discussed in Chapter 6).

Description: In species introductions, non-native species are often confronted with new niches occupied by more specialized natives, and for introduced parasites this conflict can be amplified because they also face novel hosts. Despite these obstacles, invasions of introduced parasites occur frequently, but the mechanisms that facilitate parasite invasion success are only rarely explored. Here, we investigated how the parasitic copepod Mytilicola orientalis, that recently spilled over from its principal host - the Pacific oyster Crassostrea gigas, managed to invade the niche of blue mussel Mytilus edulis intestines, which is densely occupied by its specialist congener, Mytilicola intestinalis. From field observations demonstrating invasion dynamics in nature, we designed a series of experiments addressing potential mechanisms facilitating a successful occupation of the new niche. As expected the specialist M. intestinalis can only infect mussel hosts, but displayed higher infection success there than M. orientalis in both principal host species combined. In the absence of direct competitive interactions M. orientalis compensated its lower infection success (1) by recurrent spill-over from its high-fitness reservoir oyster host, and (2) by active aggregation interference enhancing its own mating success while limiting that of M. intestinalis. The introduced parasite could thus avoid direct competition by changing its own epidemiology and indirectly decreasing the reproductive success of its competitor in the new host. Such mechanisms outside of direct competition have seldom been considered, but are crucial to understand invasion success, parasite host range and community assembly in the context of species introductions.