Host heterogeneity affects both parasite transmission to and fitness on subsequent hosts

Abstract

Infectious disease dynamics depend on the speed, number and fitness of parasites transmitting from infected hosts ('donors') to parasite-naive 'recipients'. Donor heterogeneity likely affects these three parameters, and may arise from variation between donors in traits including: (i) infection load, (ii) resistance, (iii) stage of infection, and (iv) previous experience of transmission. We used the Trinidadian guppy, , and a directly transmitted monogenean ectoparasite,, to experimentally explore how these sources of donor heterogeneity affect the three transmission parameters. We exposed parasite-naive recipients to donors (infected with a single parasite strain) differing in their infection traits, and found that donor infection traits had diverse and sometimes interactive effects on transmission. First, although transmission speed increased with donor infection load, the relationship was nonlinear. Second, while the number of parasites transmitted generally increased with donor infection load, more resistant donors transmitted more parasites, as did those with previous transmission experience. Finally, parasites transmitting from experienced donors exhibited lower population growth rates on recipients than those from inexperienced donors. Stage of infection had little effect on transmission parameters. These results suggest that a more holistic consideration of within-host processes will improve our understanding of between-host transmission and hence disease dynamics.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.

Transmission risk predicts avoidance of infected conspecifics in Trinidadian guppies

“…The predicted speed (in days) at which transmission would occur (a), and the number of parasites transmitting (b) from the stimulus fish increased through the course of infection and covaried with the avoidance behaviour they elicited. The points give the values (mean of 1,000 simulations ± 1 standard error) predicted by models built on data from 105 transmission events (from the experiment presented in Stephenson et al., ) and using the infection load, infection integral (i.e. the area under the curve of its infection load over time) and day of infection of the stimulus fish in the present experiment.…”

“…In a dichotomous choice test, uninfected guppies avoided both the visual and chemical cues, presented separately, of Gyrodactylus turnbulli‐ infected conspecifics only in the later stages of infection (Figure ). Predictions of the transmission risk posed by these infected conspecifics from models built on data from a transmission experiment using this system (Stephenson et al., ) illustrated that this avoidance behaviour tracked transmission risk through time, such that those that posed the highest predicted risk were most strongly avoided (Figure ). Our data represent unique empirical evidence that the two components of the effective contact rate β (contact rate, β c , and infectiousness, β p ) covary quantitatively, rather than as a binary comparison of infected and uninfected individuals.…”

“…To predict the transmission risk posed by the infected stimulus fish on each day of infection on which they were used as stimuli, we used models built on data from a transmission experiment using this system (for detailed methods and results see Stephenson et al., ). In brief, we experimentally infected parasite‐naïve laboratory‐bred females descended from guppies caught in the lower Aripo River, Trinidad (“donors,” n = 60), using the methods and Gt3 parasite strain described above.…”

Lost in transmission…?

“…For example, McCallum et al [11] explicitly considers interaction of the various steps involved in successful transmission from the initial infection load in an infected 'donor' host, to the dose arriving and establishing within a 'recipient' susceptible host, and proposes a general transmission framework potentially applicable to any hostparasite system. A key point to emerge from that article, and also raised by many of the other authors [2][3][4]9,10,12], is that there may be important nonlinearities and heterogeneities acting at the different stages of the overall transmission process that can alter the magnitude and functional form of transmission. Previous work has discussed the importance of nonlinearities, with respect to the contact structure between infectious and susceptible hosts (see references in [11]).…”

“…The various participants then self-assembled into sub-groups to discuss these different aspects of transmission in full over the next 3 days. The articles in this issue [1][2][3][4][5][6][7][8][9][10][11][12][13][14][15] largely represent the outcome of this process, with a few solicited to expand on areas not wholly covered at the retreat. While the list of topics represented within this issue may not be a completely exhaustive list of key topics in transmission, we believe that the broad profile of attendees has ensured that we have captured the majority of key challenges facing researchers in this field.…”