Host allometry influences the evolution of parasite host-generalism: theory and meta-analysis

Abstract

Parasites vary widely in the diversity of hosts they infect: some parasite species are specialists—infecting just a single host species, while others are generalists, capable of infecting many. Understanding the factors that drive parasite host-generalism is of basic biological interest, but also directly relevant to predicting disease emergence in new host species, identifying parasites that are likely to have unidentified additional hosts, and assessing transmission risk. Here, we use mathematical models to investigate how variation in host body size and environmental temperature affect the evolution of parasite host-generalism. We predict that parasites are more likely to evolve a generalist strategy when hosts are large-bodied, when variation in host body size is large, and in cooler environments. We then explore these predictions using a newly updated database of over 20 000 fish–macroparasite associations. Within the database we see some evidence supporting these predictions, but also highlight mismatches between theory and data. By combining these two approaches, we establish a theoretical basis for interpreting empirical data on parasites' host specificity and identify key areas for future work that will help untangle the drivers of parasite host-generalism.This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.

Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region

“…For parasites in particular, the host body size constitutes another crucial variable influencing their ecology and evolution (Guégan et al 1992;Walker et al 2017). Host body size has long been considered a determinant of parasite species richness, although it generally explains only a portion of the interspecific variance in the numbers of parasite species infecting different host species (Guégan et al 1992;Poulin 2004a;Valtonen et al 2010;Poulin and Leung 2011).…”

Lost in transmission…?

“…variation in pathogen load and stage of infection in the infectious hosts, release and survival of infective stages in the environment, susceptibility and subsequent establishment of the infecting pathogen load in the recipient host). An additional point relating to this, again raised by several of the authors [1,3,7,11,13,14], is how hard it can be to estimate transmission rates in the field. However, considering each step explicitly may help the quantification process, enabling different techniques to be used to estimate the different components, and provide clarification about which specific aspects need further investigation [11].…”

“…Similar suggestions are also raised by some of the other articles in this issue, both in multi-host [14] and single host [7] contexts. In addition, related to the ecological transmission dynamics of parasites within multi-host communities, is the evolutionary issue of whether parasites should evolve to be host generalists or specialists, and several articles addressed different aspects of this question [2,5,8,13]. A key point emerging from these articles is the importance of host-specific traits and characteristics (e.g.…”

“…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.…”

The evolution of transmission mode

“…The dependency of trade-offs on environmental conditions also needs to be considered [ 84 ]. Intriguingly, research on microsporidians in mosquitoes has shown that the factors influencing selection on vertical versus horizontal transmission include food availability and whether the parasites are embedded in co-infections [ 85 ].…”