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.

Keywords: Capsicum annuum glabriusculum; begomoviruses; biodiversity; plant–virus interactions; population genetic diversity; recombination.

Figure 1.

Location of sampled chiltepin populations. Map shows the location of populations from wild (W), let-standing (L), and cultivated (C) populations within six biogeographical provinces in Mexico. Number of PepGMV and PHYVV sequences from each location is shown between parentheses. Full names of each location can be found in Supplementary Table S2.

Figure 2.

Distribution and abundance of recombination breakpoints in both the DNA-A and the DNA-B of PepGMV and PHYVV. x axis indicates the position (nt) of each intra-specific (blue line) and inter-specific (red line) recombination breakpoint in each component of the viral genome. Colored arrows denote the position and orientation of each gene. CP, blue; REn, green; TrAP, yellow; Rep, red; NSP, purple; MP, orange. y axis indicates the number of virus isolates in which each recombination breakpoint was detected.

Figure 3.

Composite phylogenies of the DNA-A and DNA-B of PepGMV and PHYVV. Lines denote isolates with significant (green) and non-significant (red) phylogenetic congruence between DNA-A and DNA-B as detected by CopyCat. Isolates are identified by a three-letter code indicating the chiltepin population (see Supplementary Table S2) followed by the number of the sample, a one-letter code indicating the level of human management (C, cultivated; L, let-standing; W, wild) and the year of collection.

Figure 4.

Bivariate relationships between ecological and epidemiological factors of chiltepin populations and evolutionary parameters of PepGMV populations. Significant regressions of plant species richness, chiltepin genetic diversity and plant density, and PepGMV prevalence onto the genetic diversity, the rate of non-synonymous and synonymous substitutions, the frequency of recombinants, and the frequency of different recombinant profiles in PepGMV populations are represented for each genomic component: DNA-A (blue) and DNA-B (red). Species richness (SR) is expressed as number of species; host genetic diversity (H_e) is expressed as expected heterozygosity; host plant density is expressed as plants/m², and virus prevalence as percentage of infected plants over the total of plants sampled. Note the different scales in the x- and y axis depending on the factor-parameter combination. Data correspond to eight populations with at least four fully sequenced viral isolates.