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

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.

Genetically depauperate and still successful: few multilocus genotypes of the introduced parthenogenetic weevil Naupactus cervinus (Coleoptera: Curculionidae) prevail in the Continental United States

“…The main objective is to test the hypothesis that the one successful invader lineage found worldwide will also be identified as the most prevalent (and therefore successful) across the continental United States. Indeed, if this were the case this could support the notion that this successful lineage can thrive in a diversity of habitats and feed on a variety of taxing host-plants, possibly due to pre-existing adaptations (Rodriguero et al 2019) and/or due to plasticity in gene expression variation related to the exploitation of a variety of food sources (Mackay et al 2021).…”

“…It is puzzling that another parthenogenetic species, the whitefringed weevil Naupactus leucoloma, with the same evolutionarily favorable core shared gene expression regime for responding to different types of stressful situations as N. cervinus (Mackay et al 2021) has only established introduced populations in suitable areas (Guzmán et al 2012), signaling that the Fuller's rose weevil is a superior colonizer. Thus, N. cervinus must have another source of adaptive evolution in addition to expression plasticity: together with epigenetic variation compensating for decreased genetic variation, the success of the Fuller's rose weevil may also have a genetic basis.…”

“…Explorations of the transcriptional plasticity of introduced populations of N. cervinus in the US and the native range have revealed intriguing patterns of host-specific expression and modulated responses to plant defenses (Mackay-Smith et al 2021). For example, significantly different quantities of immune defense, detoxification and host detection genes were found to be up-regulated in legume-feeding weevils when compared to those feeding on other hosts.…”

Genetically Depauperate and Still Successful: Few Multilocus Genotypes of the Introduced Parthenogenetic Weevil Naupactus cervinus (Coleoptera: Curculionidae) Prevail in the Continental United States

“…The main objective is to test the hypothesis that the one successful invader lineage found worldwide will also be identified as the most prevalent (and, therefore, successful) across the continental US. Indeed, if this were the case, this might support the notion that this successful lineage can thrive in a diversity of habitats and feed on a variety of taxing host plants, possibly due to pre-existing adaptations [ 20 ] and/or due to plasticity in gene expression variation related to the exploitation of a variety of food sources [ 31 ].…”

“…In contrast, populations within the introduced range are not expected to harbor significant levels of genetic variation, given that males have never been detected in any area of the introduced range and that introductions are recent, most probably following bottlenecks. However, explorations of the transcriptional plasticity of introduced populations of N. cervinus in the US and the native range have revealed intriguing patterns of host-specific expression and modulated responses to plant defenses [ 31 ]. For example, significantly different quantities of immune defense, detoxification, and host detection genes were found to be up-regulated in legume-feeding weevils, when compared to those feeding on other hosts.…”