- Eco-Immunology, Institute of Integrative Biology/University of Liverpool, Liverpool, United Kingdom
- Behavior & Social Evolution, Bioinformatics & Computational Biology, Evolutionary Ecology, Expression Studies
Trait-specific trade-offs prevent niche expansion in two parasites
Trade-offs in fitness components and ecological source-sink dynamics affect host specialisation in two parasites of Artemia shrimps
Ecological specialisation, especially among parasites infecting a set of host species, is ubiquitous in nature. Host specialisation can be understood as resulting from trade-offs in parasite infectivity, virulence and growth. However, it is not well understood how variation in these trade-offs shapes the overall fitness trade-off a parasite faces when adapting to multiple hosts. For instance, it is not clear whether a strong trade-off in one fitness component may sufficiently constrain the evolution of a generalist parasite despite weak trade-offs in other components. A second mechanism explaining variation in specialisation among species is habitat availability and quality. Rare habitats or habitats that act as ecological sinks will not allow a species to persist and adapt, preventing a generalist phenotype to evolve. Understanding the prevalence of those mechanisms in natural systems is crucial to understand the emergence and maintenance of host specialisation, and biodiversity in general.
In their study "Trait-specific trade-offs prevent niche expansion in two parasites", Lievens et al.  report the results of an evolution experiment involving two parasitic microsporidians, Anostracospora rigaudi and Enterocytospora artemiae, infecting two sympatric species of brine shrimp, Artemia franciscana and Artemia parthenogenetica. The two parasites were originally specialised on their primary host: A. rigaudi on A. parthenogenetica and E. artemiae on A. franciscana, although they encounter both species in the wild but at different rates. After passaging each parasite on each single host and on both hosts alternatively, Lievens et al. asked how host specialisation evolved. They found no change in specialisation at the fitness level in A. rigaudi in either treatment, while E. artemiae became more of a generalist after having been exposed to its secondary host, A. parthenogenetica. The most interesting part of the study is the decomposition of the fitness trade-off into its underlying trade-offs in spore production, infectivity and virulence. Both species remained specialised for spore production on their primary host, interpreted as caused by a strong trade-off between hosts preventing improvements on the secondary host. A. rigaudi evolved reduced virulence on its primary host without changes in the overall fitness trad-off, while E. artemiae evolved higher infectivity on its secondary host making it a more generalist parasite and revealing a weak trade-off for this trait and for fitness. Nevertheless, both parasites retained higher fitness on their primary host because of the lack of an evolutionary response in spore production.
This study made two important points. First, it showed that despite apparent strong trade-off in spore production, a weak trade-off in infectivity allowed E. artemiae to become less specialised. In contrast, A. rigaudi remained specialised, presumably because the strong trade-off in spore production was the overriding factor. The fitness trade-off that results from the superposition of multiple underlying trade-offs is thus difficult to predict, yet crucial to understand potential evolutionary outcomes. A second insight is related to the ecological context of the evolution of specialisation. The results showed that E. artemiae should be less specialised than observed, which points to a role played by source-sink dynamics on A. parthenogenetica in the wild. The experimental approach of Lievens et al. thus allowed them to nicely disentangle the various sources of constraints on the evolution of host adaptation in the Artemia system.
 Lievens, E.J.P., Michalakis, Y. and Lenormand, T. (2019). Trait-specific trade-offs prevent niche expansion in two parasites. bioRxiv, 621581, ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/621581