The effect of ecosystem biodiversity on virus genetic diversity depends on virus species: A study of chiltepin-infecting begomoviruses in Mexico

Abstract

Current declines in biodiversity put at risk ecosystem services that are fundamental for human welfare. Increasing evidence indicates that one such service is the ability to reduce virus emergence. It has been proposed that the reduction of virus emergence occurs at two levels: through a reduction of virus prevalence/transmission and, as a result of these epidemiological changes, through a limitation of virus genetic diversity. Although the former mechanism has been studied in a few host-virus interactions, very little is known about the association between ecosystem biodiversity and virus genetic diversity. To address this subject, we estimated genetic diversity, synonymous and non-synonymous nucleotide substitution rates, selection pressures, and frequency of recombinants and re-assortants in populations of Pepper golden mosaic virus (PepGMV) and Pepper huasteco yellow vein virus (PHYVV) that infect chiltepin plants in Mexico. We then analyzed how these parameters varied according to the level of habitat anthropization, which is the major cause of biodiversity loss. Our results indicated that genetic diversity of PepGMV (but not of PHYVV) populations increased with the loss of biodiversity at higher levels of habitat anthropization. This was mostly the consequence of higher rates of synonymous nucleotide substitutions, rather than of adaptive selection. The frequency of recombinants and re-assortants was higher in PepGMV populations infecting wild chiltepin than in those infecting cultivated ones, suggesting that genetic exchange is not the main mechanism for generating genetic diversity in PepGMV populations. These findings provide evidence that biodiversity may modulate the genetic diversity of plant viruses, but it may differentially affect even two closely related viruses. Our analyses may contribute to understanding the factors involved in virus emergence.

The impact of host genetic diversity on virus evolution and emergence

“…), although the absence of such effect has been reported (Rodelo‐Urrego et al . ). Also, analyses of host‐parasite co‐evolution have revealed a positive association between host and parasite genetic diversity (Paterson et al .…”

Ecological Factors Affecting Infection Risk and Population Genetic Diversity of a Novel Potyvirus in Its Native Wild Ecosystem

“…In contrast, agroecosystems are often dominated by annual plants – or managed as such –, and viruses adapted to wild perennials may over-compete crop viruses ( Wren et al, 2006 ; Roossinck, 2010 ). In addition, human management of the host population has a great impact on plant virus populations ( Pagán et al, 2012 ; Alexander et al, 2014 ; Rodelo-Urrego et al, 2015 ), so that plant viruses native from wild ecosystems may have different population dynamics than those typical in agroecosystems. Consequently, the factors driving the infection risk and population genetic diversity might be different than those identified for crop viruses ( Fraile et al, 2017 ).…”

Ecological determinants of Potyvirus emergence in wild ecosystems

“…This indicates that neutral evolution, rather than adaptive selection, might be responsible for the changes in MeRV population genetic diversity associated with fluctuations in virus prevalence. Similar results have been obtained in other plant virus populations infecting wild hosts(Lima et al, 2013;Rodelo-Urrego et al, 2015).The results of the model selection analyses for WHMV population genetic diversity are more difficult to interpret. The most important factors predicting virus population haplotype and genetic diversity were host plant relative abundance and rainfalls.…”

“…For instance, host genetic diversity or vector population dynamics has been also reported as important determinants of virus disease risk and population genetic diversity in wild ecosystems (Pagán et al, 2012;Rodelo-Urrego et al, 2015;Rodríguez-Nevado et al, 2018). Unfortunately, the lack of information on the genomic sequence of most potyvirus hosts identified in this thesis prevented including this variable in our analyses.…”

“…RNA viruses, as are potyviruses, may differ greatly in their modes of macro and microevolution (Kitchen et al, 2011), and ecological factors are thought to shape these processes (Huyse et al, 2005). However, little is known about which and how ecological factors shape virus population genetic diversity at both evolutionary scales (Huyse et al, 2005;Rodelo-Urrego et al, 2015).…”