bioRxiv Science⌕ Search

bioRxiv · 10.1101/2022.09.30.510290

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

Abstract

BackgroundDivergent 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. ResultsPrincipal 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 DXY and FST while the Z chromosome loci had decreased DXY and increased FST. ConclusionThese 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.

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Fiteni, E., Durand, K., Gimenez, S., Meagher, R. L., Legeai, F., Kergoat, G. J., Negre, N., d'Alencon, E., NAM, K.. 2022-10-03. Host-plant adaptation as a driver of incipient speciation in the fall armyworm (Spodoptera frugiperda). https://doi.org/10.1101/2022.09.30.510290

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

Global homeostatic forces shape the composition of a hyperdiverse tropical insect fauna

Despite comprising the bulk of terrestrial biodiversity, we know surprisingly little about insect faunas, particularly in the tropics. Here, we characterize the insect fauna of Madagascar, a global biodiversity hotspot, based on extensive DNA metabarcoding of Malaise trap and leaf litter samples. We estimate that the fauna comprises at least 250,000 species, only 5% of which are currently recorded. The ecological and taxonomic composition is surprisingly similar to that of temperate forests. We show that this is likely caused by global homeostatic forces shaping net diversification rates after colonization of Madagascar rather than by the composition of colonizing lineages. Features differing from temperate forests include the dearth of parasitoids and richness of beetles. Understanding the forces shaping these patterns is key in sustainable management of tropical insect faunas.

evolutionary biology↗

Do divergent mitochondrial backgrounds alter the fate of nuclear alleles during hybridization and admixture?

Hybridization brings together genetic variation from different populations or species into admixed genomes. As selection sorts this variation, the fate of each allele is determined by its fitness effect in the new hybrid genomic background. Because mitochondrial genes coevolve with the nuclear genome, they may be especially sensitive to foreign nuclear backgrounds, making them potential "hot-spots" for hybrid incompatibilities. Here, we test whether selection against mitonuclear incompatibilities drives repeatable hybridization outcomes. Specifically, we experimentally evolved three sets of five populations of hybrid Drosophila melanogaster, each carrying the same nuclear chromosomes but paired with one of three increasingly divergent mitochondrial DNA backgrounds. We hypothesized that accumulated incompatibilities would result in different patterns of nuclear admixture among mitochondrial backgrounds. To test this, we tracked nuclear allele frequencies in all 15 populations by whole-genome sequencing at intermediate time points. After 25 generations, we observed that rapid genomic evolution produced a strikingly parallel mosaic of both nuclear ancestries, independent of mitochondrial background. Contrary to our hypothesis, we found no evidence that mitochondrial background1 shaped nuclear admixture, even for interspecific combinations. These results suggest that in species with large effective population sizes, efficient purifying selection limits the accumulation of mitonuclear incompatibilities, allowing selection on nuclear alleles to promote repeatable ancestry sorting immediately following hybridization.

evolutionary biology↗

Body size cascades from Neodiprion sawfly hosts to Perilampid parasitoids: An investigation of sequential divergence

Ecological speciation drives diversity in plant-eating insect systems, but it may also generate parallel specialization in parasitoid associates in a cascading effect of "sequential divergence." However, sequential divergence has never been successfully identified in parasitoids of externally feeding insects. To address this gap, we consider the Pinus-Neodiprion-Perilampus neodiprioni system, where plant-associated, externally feeding Neodiprion demonstrate ecological divergence, as supported by body size as a magic trait in sympatric species. It seems possible that this body size differentiation may cascade to Neodiprion's parasitoids via sequential divergence. Therefore, we asked, "Does P. neodiprioni exhibit host-specific divergence in body size that parallels patterns in Neodiprion hosts?" Further, "Does P. neodiprioni exhibit host-related variation in the abdominal region or sexually dimorphic features, supporting reproductive barriers?" Using by-catch samples, we measured body size of P. neodiprioni, reared from Neodiprion lecontei and Neodiprion pinetum hosts. We analyzed body size variation as predicted by host species, parasitoid sex, host sex, host cocoon size, latitude, and their interactions. In addition, we used mixed models to analyze the effects of parasitoid sex and Neodiprion host on three size-based facial features. We found that P. neodiprioni demonstrates host-associated body size variation that mirrors size differences in their Neodiprion hosts. In addition, host-associated size variation occurs in the abdominal region and two sexually dimorphic characters of P. neodiprioni, supporting possible reproductive isolation. Together, these patterns suggest that host magic traits may drive not only within-species ecological divergence, but they can facilitate parasitoids' subsequent morphological differentiation and possible sequential divergence.

evolutionary biology↗