An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts

Abstract

21Understanding the occurrence and spatial spread of infectious disease is a major challenge to 22 epidemiologists and evolutionary biologists. Current theory predicts the spread of highly 23 exploitative parasites at the front of spreading epidemics. However, many parasites rely on the 24 dispersal of their hosts to spread to new habitats. This may lead to a conflict between local 25 transmission and spatial spread, counteracting selection for highly virulent parasites. Yet, there 26 are no experimental tests of these hypotheses. Here we investigate parasite evolution in an 27 experiment creating conditions in cores and at fronts of spreading host-parasite populations, 28 using the freshwater host Paramecium caudatum and its bacterial parasite Holospora undulata. 29 We find that parasites from experimental range fronts induce higher rates of host dispersal than 30 parasites from the core. This divergence is accompanied by lower levels of virulence and 31 delayed development of infectious stages of front parasites. We validate these experimental 32 results by fitting an epidemiological model to time-series data independently obtained from the 33 experiment. This combined evidence suggests an evolutionary trade-off between host 34 exploitation (virulence) and host-mediated dispersal, resulting in a shift of the investment in 35 horizontal transmission. In conclusion, our results show that different segments of an epidemic 36 wave may be under divergent selection pressures, shaping the evolution of parasite life history. 37 These findings have important implications for our understanding of the interaction between 38 demography and rapid evolutionary change in spreading populations, which is crucial for the 39 management of emerging diseases, biological invasions and other non-equilibrium scenarios.40 41 42 43 2016; Penczykowski et al., 2016). In spatially homogeneous populations, theory often predicts 48 the spread of highly exploitative (i.e., virulent) parasites with a high transmission potential 49 (Andre and Hochberg, 2005). Outbreaks of disease in the wild, however, generally occur in 50 highly dynamic or patchy host populations, such as in metapopulations or in range expanding 51 and invasive species. Since many parasites spread to new habitats via host-mediated dispersal, 52 the evolution of such parasites will now depend not only on the strategies that maximise 53 transmission in response to changes in host demography (Nørgaard et al., 2019a; Penczykowski 54 et al., 2016), but also on a correlated response to the spatial sorting of hosts with different 55 dispersal capacities across a landscape (see (Calcagno et al., 2006; Perkins et al., 2013). 56 However, how the increased mobility of a host during range expansion processes (Phillips et 57 al., 2010) translates into the emergence and spread of infectious disease, remains unclear due 58 to the high complexity of ecological and evolutionary dynamics at play (see (Dunn and 59 Hatcher , 2015; Perkins et al., 2008; Torchin et al., 2003). 60By explori...

Parasitism and host dispersal plasticity in an aquatic model system

“…More specifically, in a host-parasite system, prevalence could be a good predictor of a patch future condition only at high parasite virulence (Deshpande et al, 2020). In our system, Holospora undulata generally reduces survival and reproductive success of P. caudatum (Restif & Kaltz, 2006;Nørgaard et al, 2020), which is also reflected by differences in population density between uninfected control and infected microcosms in the present experiment (density uninfected control: 288 mL -1 , ± 103; infected: 139 mL -1 , ± 91 SE). Hence, we might speculate that some strains could have had an evolutionary history with a highly virulent parasite in the wild.…”

“…In our analysis we observed that the dispersal outcome was affected by the identity of the host strains ( Figure 1A-B). Previous studies reported that infection by H. undulata reduced dispersal in P. caudatum (Fellous et al, 2011;Nørgaard et al, 2020), which was related to a reduction in survival and reproduction. The explanation for a reduced dispersal can easily be connected to the negative effect that a parasite may have on its host locomotory ability (Horky et al, 2014;Binning et al, 2017).…”

“…In parallel, three uninfected controls for each strain were maintained (total of 180 replicates). Using the methods described in Nørgaard et al (2020), dispersal of infected and uninfected control replicates was tested three weeks postinfection, when population size (mean: 190 mL -1 ± 9 SE; 95% range [172; 208]) and infection prevalence (mean: 26.8 % ± 2.1; 95% range [3.1; 90.7]) had settled naturally in each experimental replicate. Shortly, the dispersal arena consisted of three 50-mL Falcon tubes, one in the middle connected to two lateral tubes.…”

“…Infectious spores are immobile and therefore rely on host movement or water current for their own dispersal. Infection reduces P. caudatum survival (Restif & Kaltz, 2006) and dispersal (Fellous et al, 2011;Nørgaard et al, 2020).…”

The partitioning of symbionts effects on host resource acquisition and developmental plasticity

“…Individuals hence allocate 20 limited amounts of energy to some traits at the detriment of others (Stearns 1989). Many 21 examples of such trade-offs have been thoroughly documented in various organisms ranging 22 from plants to microorganisms (Lind et al 2013;Nørgaard et al 2020). For example, lifespan 23 and reproductive rate are constrained by a trade-off (Chippindale et al 2004;Flatt 2011;24 Travers, Garcia-Gonzalez and Simmons 2015) because endogenous resources allocated to 25 reproductive functions are not available for somatic and repair functions (Flatt, 2011;26 Schwenke, Lazzaro and Wolfner, 2016).…”