Can pathogens optimize both transmission and dispersal by exploiting sexual dimorphism in their hosts?

Nørgaard, Louise Solveig; Phillips, Benjamin L.; Hall, Matthew D.

doi:10.1098/rsbl.2019.0180

Cited by 13 publications

(10 citation statements)

References 29 publications

(51 reference statements)

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“…Male and female Daphnia differ in many characteristics that potentially relate to their capacity to cope with both thermal stress and pathogen infection, as demonstrated here for body size (average size: males 2.39 mm, females 3.50 mm) and the control of pathogen proliferation (average spore production: males 0.92 million, females 3.16 million), and in other studies for traits such as the infection‐induced increase in late‐life mortality (Gipson & Hall, 2018; Gipson et al., 2019) and changes in host movement (Nørgaard et al., 2019). Our results, however, show that the greater reduction in thermal limits that females suffer when infected persists even after correcting for overt sex differences in relative body size and the control of pathogen proliferation.…”

Section: Resultssupporting

confidence: 76%

Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits

Laidlaw

Hector

Sgrò

et al. 2020

Ecology and Evolution

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The climate is warming at an unprecedented rate, pushing many species toward and beyond the upper temperatures at which they can survive. Global change is also leading to dramatic shifts in the distribution of pathogens. As a result, upper thermal limits and susceptibility to infection should be key determinants of whether populations continue to persist, or instead go extinct. Within a population, however, individuals vary in both their resistance to both heat stress and infection, and their contributions to vital growth rates. No more so is this true than for males and females. Each sex often varies in their response to pathogen exposure, thermal tolerances, and particularly their influence on population growth, owing to the higher parental investment that females typically make in their offspring. To date, the interplay between host sex, infection, and upper thermal limits has been neglected. Here, we explore the response of male and female Daphnia to bacterial infection and static heat stress. We find that female Daphnia, when uninfected, are much more resistant to static heat stress than males, but that infection negates any advantage that females are afforded. We discuss how the capacity of a population to cope with multiple stressors may be underestimated unless both sexes are considered simultaneously.

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Section: Resultssupporting

confidence: 76%

Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits

Laidlaw

Hector

Sgrò

et al. 2020

Ecology and Evolution

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“…However, we find little evidence for manipulation to increase the dispersal. Consistent with previous observations of negative effects of infection in this ( 59) and other systems (36,(60)(61)(62), core parasites reduced host dispersal, whereas infection with front parasites produced levels of dispersal comparable to uninfected Paramecium. Path analysis indicates that virulence is the main direct predictor of host dispersal in our assays.…”

Section: Trait Relationships: Proximate Causes Of Infected Dispersal Ratesupporting

confidence: 91%

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

et al. 2021

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Exploitative parasites are predicted to evolve in highly connected populations or in expanding epidemics. However, many parasites rely on host dispersal to reach new populations, potentially causing conflict between local transmission and global spread. We performed experimental range expansions in interconnected microcosms of the protozoan Paramecium caudatum, allowing natural dispersal of hosts infected with the bacterial parasite Holospora undulata. Parasites from range front treatments facilitated host dispersal and were less virulent, but also invested less in horizontal transmission than parasites from range cores. These differences were consistent with parameter estimates derived from an epidemiological model fitted on population‐level time‐series data. Our results illustrate how dispersal selection can have profound consequences for the evolution of parasite life history and virulence. Decrypting the eco‐evolutionary processes that shape parasite 'dispersal syndromes' may be important for the management of spreading epidemics in changing environments, biological invasions or in other spatial non‐equilibrium settings.

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“…However, we find little evidence for manipulation to increase the dispersal. Consistent with previous observations of negative effects of infection in this (59) and other systems (36,(60)(61)(62), core parasites reduced host dispersal, whereas infection with front parasites produced levels of dispersal comparable to uninfected Paramecium. Path analysis indicates that virulence is the main direct predictor of host dispersal in our assays.…”

Section: Trait Relationships: Proximate Causes Of Infected Dispersal supporting

confidence: 91%

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

Noergaard

Zilio

Saade

et al. 2020

Preprint

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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...

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Can pathogens optimize both transmission and dispersal by exploiting sexual dimorphism in their hosts?

Cited by 13 publications

References 29 publications

Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits

Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits

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

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

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