Host-plant adaptation as a driver of incipient speciation in the fall armyworm (Spodoptera frugiperda)

Abstract

Background: Divergent selection on host-plants is one of the main evolutionary forces driving ecological speciation in phytophagous insects. The ecological speciation might be challenging in the presence of gene flow and assortative mating because the direction of divergence is not necessarily the same between ecological selection (through host-plant adaptation) and assortative mating. The fall armyworm (FAW), a major lepidopteran pest species, is composed of two sympatric strains, corn and rice strains, named after two of their preferred host-plants. These two strains have been hypothesized to undergo incipient speciation, based on (i) several lines of evidence encompassing both pre- and post-zygotic reproductive isolation, and (ii) the presence of a substantial level of genetic differentiation. Even though the status of these two strains has been established a long time ago, it is still yet to be found whether these two strains indeed exhibit a marked level of genetic differentiation from a large number of genomic loci. Here, we analyzed whole genome sequences from 56 FAW individuals either collected from pasture grasses (a part of the favored host range of the rice strain) or corn to assess the role of host-plant adaptation in incipient speciation.

Results: Principal component analysis of whole genome data shows that the pattern of divergence in the fall armyworm is predominantly explained by the genetic differentiation associated with host-plants. The level of genetic differentiation between corn and rice strains is particularly marked in the Z chromosome. We identified one autosomal locus and two Z chromosome loci targeted by selective sweeps specific to rice strain and corn strain, respectively. The autosomal locus has both increased D_XY and F_ST while the Z chromosome loci had decreased D_XY and increased F_ST.

Conclusion: These results show that the FAW population structure is dominated by the genetic differentiation between corn and rice strains. This differentiation involves divergent selection targeting at least three loci, which include a locus potentially causing reproductive isolation. Taken together, these results suggest the evolutionary scenario that host-plant speciation is a driver of incipient speciation in the fall armyworm.

Keywords: Fall armyworm; Host-plant adaptation; Incipient speciation; Speciation with gene flow; Spodoptera frugiperda.

Fig. 1

Genetic differentiation between host-plants and strains. Principal component analysis from A whole nuclear genome, B the Z chromosome, and C autosomes. TPI-sfC and TPI-sfR represent strains identified from the TPI marker. The red and blue points indicate samples collected from corn fields and pasture grasses, respectively

Fig. 2

Genetic differentiation between groups in the FAW. A F_ST was calculated between the corn group and the grass group. (left) The histogram shows F_ST calculated from random groups. The red vertical bar indicates F_ST calculated between the corn group and the grass group. (middle) F_ST calculated in 500 kb windows was shown for each chromosome. (right) The histogram of F_ST was calculated in 500 kb windows. The black vertical bar indicates F_ST = 0. B F_ST was calculated between two groups with different mitochondrial markers within the corn group. Please note that A and B have different ranges of F_ST in the rightmost panels

Fig. 3

Selectively targeted loci. The composite likelihood of selective sweep along the genome was calculated from the corn or grass group. Obvious outliers of likelihood were indicated by asterisks

Fig. 4

Loci under divergent selective sweeps. D_XY (upper) and F_ST (lower) were calculated from the targets of selective sweep specific to the grass group (the red rectangles) and the corn group (the blue rectangles)

Fig. 5

An evolutionary scenario of speciation in the fall armyworm. (i) Divergence selection on a locus on chromosome 12 caused reproductive isolation by reducing gene flow between ancestral corn and grass groups. The ancestral corn group experienced divergent selection on the Z chromosome as well. As a consequence, the corn group (sfC) and the grass group (sfR) had differentiated ranges of host-plants. (ii) Evolutionary forces split the corn group (sfC) into two sub-groups, mt-A and mt-B, with different mitochondrial markers