Does genetic diversity protect host populations from parasites? A meta-analysis across natural and agricultural systems

Abstract

If parasites transmit more readily between closely related hosts, then parasite burdens should decrease with increased genetic diversity of host populations. This important hypothesis is often accepted at face value—notorious epidemics of crop monocultures testify to the vulnerability of host populations that have been purged of diversity. Yet the relationship between genetic diversity and parasitism likely varies across contexts, differing between crop and noncrop hosts and between experimental and natural host populations. Here, we used a meta‐analytic approach to ask if host diversity confers protection against parasites over the range of contexts in which it has been tested. We synthesized the results of 102 studies, comprising 2004 effect sizes representing a diversity of approaches and host‐parasite systems. Our results validate a protective effect of genetic diversity, while revealing significant variation in its strength across biological and empirical contexts. In experimental host populations, genetic diversity reduces parasitism by ∼20% for noncrop hosts and by ∼50% for crop hosts. In contrast, observational studies of natural host populations show no consistent relationship between genetic diversity and parasitism, with both strong negative and positive correlations reported. This result supports the idea that, if parasites preferentially attack close relatives, the correlation of genetic diversity with parasitism could be positive or negative depending upon the potential for host populations to evolve in response to parasite selection. Taken together, these results reinforce genetic diversity as a priority for both conservation and agriculture and emphasize the challenges inherent to drawing comparisons between controlled experimental populations and dynamic natural populations.

Infectious disease in an era of global change

“…Increased population connectivity can also enable pathogens and their vectors to shift to novel host species, from infected mosquitoes travelling on boats or in planes to agricultural pathogens being inadvertently relocated. Hosts that have not previously been exposed to such pathogens, and thus have no co-evolved defences, yet are phylogenetically and/or genetically similar to the original host are often most at risk 139 , 140 , a fact that makes homogenization of crops 141 or livestock a concern. Novel pathogen introductions can have large-scale population and ecosystem impacts, of which one famous example is the extirpation of the American chestnut tree by chestnut blight 142 .…”

Mosaic vaccination: How distributing different vaccines across a population could improve epidemic control

“… 2020 ) and natural systems (Ekroth et al. 2019 ), especially those in which rapid host evolution is unlikely (Gibson and Nguyen 2020 ). Our work suggests that vaccination strategies that harness—and, in fact, generate—variation can often outperform conventional vaccines.…”

Mosaic vaccination: how distributing different vaccines across a population could improve epidemic control

“…This mosaic strategy generates heterogeneity in the host population (and, thus, the fitness landscape for pathogens), which has long been thought to be protective against disease outbreaks [39]. Theory predicts that ‘naturally’ variable host populations are less likely to experience sustained disease spread (e.g., [34, 35]), and the protective effect of host variation has been empirically demonstrated in a number of experimental (e.g., [40, 41]) as well as natural systems [42], especially those in which rapid host evolution is unlikely [43]. Our work suggests that vaccination strategies that harness—and, in fact, generate—variation can often outperform conventional vaccines.…”