Contrasting population structure and demographic history of cereal aphids in different environmental and agricultural landscapes

Abstract

Genetic diversity of populations has important ecological and evolutionary consequences, whose understanding is fundamental to improve the sustainability of agricultural production. Studies of how differences in agricultural management and environment influence the population structure of insect pests are central to predict outbreaks and optimize control programs. Here, we have studied the population genetic diversity and evolution of Sitobion avenae and Sitobion miscanthi, which are among the most relevant aphid pests of cereals across Europe and Asia, respectively. We have used genotyping by sequencing (GBS) to identify genome-wide single nucleotide polymorphisms (SNPs) to infer the geographic structure and migration patterns. In the present study, we show that the population structure in present-day populations is different from that described in previous studies, which suggest that they have evolved recently possibly as a response to human-induced changes in agriculture. This study shows that S. avenae in England is predominantly parthenogenetic and there has been a demographic and spatial expansion of a single genetic cluster, which could correspond with the insecticide resistance superclone identified in previous studies. Conversely, in China, S. miscanthi populations are mostly cyclical parthenogenetic, with one sexual stage in autumn to produce overwintering eggs, and there are six genetically differentiated subpopulations and high genetic differentiation between geographic locations, which suggests that further taxonomical research is needed. Unlike S. avenae in England, there is no evidence for insecticide resistance and there is no predominance of a single lineage in S. miscanthi in China.

Keywords: China; England; cereal aphids; insecticide resistance; population genetics.

FIGURE 1

Maps showing the locations where samples of S. avenae were collected in England (a) and where S. miscanthi aphids were collected in China (b)

FIGURE 2

Structure analysis based on 14,520 SNPs across 10 Chinese populations, with K = 6. Each bar represents one individual and the colors of the bars the posterior probability that each belongs to one of the six genetic clusters. GC1—blue; GC2—magenta; GC3—yellow; GC4—green; GC5—purple; GC6—red

FIGURE 3

Midpoint rooted phylogenetic tree estimated with RAxML for the S. miscanthi phased haplotypes from China using a dataset of 14,520 SNPs. The six genetic clusters are highlighted with different colors, corresponding to the colors in the barplot of Figure 2. Labels on branches are bootstrap values >90%. GC1—blue; GC2—magenta; GC3—yellow; GC4—green; GC5—purple; GC6—red

FIGURE 4

Structure analysis based on 846 SNPs across 12 English populations of S. avenae for K = 2. Each bar represents one individual and the colors of the bars the posterior probability that each belongs to each of the genetic clusters

FIGURE 5

Midpoint rooted phylogenetic tree estimated with RAxML for the S. avenae phased haplotypes from England using a dataset of 846 SNPs. The two‐phased multimarker haplotypes from every individual are colored in red and green, and the clades have been collapsed except for the earliest branching haplotype of each clade. Labels on branches are bootstrap values >90%