Host-specific gene expression as a tool for introduction success in Naupactus parthenogenetic weevils.

Ava Mackay-Smith,Marcela Rodriguero,Analia A Lanteri,Anna Okimoto,Andrea S Sequeira,Rosalind Lucier,Mary Kate Dornon,Flavia Mendonca De Sousa,Viviana Confalonieri,J Joe Hull

doi:10.1371/journal.pone.0248202

Ava Mackay-Smith, Marcela Rodriguero + Show 8 more

Open Access

https://doi.org/10.1371/journal.pone.0248202

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Abstract

Food resource access can mediate establishment success in invasive species, and generalist herbivorous insects are thought to rely on mechanisms of transcriptional plasticity to respond to dietary variation. While asexually reproducing invasives typically have low genetic variation, the twofold reproductive capacity of asexual organisms is a marked advantage for colonization. We studied host-related transcriptional acclimation in parthenogenetic, invasive, and polyphagous weevils: Naupactus cervinus and N. leucoloma. We analyzed patterns of gene expression in three gene categories that can mediate weevil-host plant interactions through identification of suitable host plants, short-term acclimation to host plant defenses, and long-term adaptation to host plant defenses and their pathogens. This approach employed comparative transcriptomic methods to investigate differentially expressed host detection, detoxification, immune defense genes, and pathway-level gene set enrichment. Our results show that weevil gene expression responses can be host plant-specific, and that elements of that response can be maintained in the offspring. Some host plant groups, such as legumes, appear to be more taxing as they elicit a complex gene expression response which is both strong in intensity and specific in identity. However, the weevil response to taxing host plants shares many differentially expressed genes with other stressful situations, such as host plant cultivation conditions and transition to novel host, suggesting that there is an evolutionarily favorable shared gene expression regime for responding to different types of stressful situations. Modulating gene expression in the absence of other avenues for phenotypic adaptation may be an important mechanism of successful colonization for these introduced insects.

Highlights

Invasiveness and diet breadthPrevailing theories suggest that the majority of non-native species introduced to new habitats fail to establish due to travel stress, climate incompatibility, inadequate or inappropriate food resources, or small population size, among other factors [1]
Legume host plants generate large transcriptional responses. For both N. cervinus and N. leucoloma, there were significantly more upregulated host detection (HD), detoxification (DTX), and immune defense (IM) genes in weevils feeding on legume host plants (Fig 1i)
When exploring the interaction of tissue effects and functional group effects on differentially expressed gene (DEG) differences between host plants, we found that both factors significantly impacted the expression of DTX genes only in N. cervinus

Summary

Introduction

Prevailing theories suggest that the majority of non-native species introduced to new habitats fail to establish due to travel stress, climate incompatibility, inadequate or inappropriate food resources, or small population size, among other factors [1]. If it is true that legume and citrus hosts are more resource-taxing to herbivores compared to other hosts, it could be expected that herbivores that feed on highly chemically defended species will have more species-specific transcriptional responses, and that the weevils consuming these host plants have acclimated to these defenses Because of this acclimation, we predicted larger numbers of unique expression patterns between weevils feeding on citrus members (Rutaceae), and between those feeding on legume members (Fabaceae), than between those feeding on members of a non-citrus, nonlegume group (Asteraceae), even though the degrees of phylogenetic relatedness between host plants within each family are not equivalent. Exploration of global expression patterns in all host plants and experimental contrasts It is entirely possible that important aspects of weevil acclimation and/or adaptation to feeding on resource-taxing host plants, or on novel hosts, may involve differential regulation of genes beyond the three targeted gene categories of detection, detoxification and immune response. We found commonalities to the response of taxing host plants and other stressful situations such as host plant cultivation conditions and/or a transition to a novel host

Results

Discussion

Experimental procedures Weevil collection and rearing