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

Naupactus cervinus is a parthenogenetic weevil native to South America that is currently distributed worldwide. This flightless species is polyphagous and capable of modifying gene expression regimes for responding to stressful situations. Naupactus cervinus was first reported in the continental United States in 1879 and has rapidly colonized most of the world since. Previous studies suggested that an invader genotype successfully established even in areas of unsuitable environmental conditions. In the present work, we analyze mitochondrial and nuclear sequences from 71 individuals collected in 13 localities across three states in the southern US, in order to describe the genetic diversity in this area of introduction that has not yet been previously studied. Our results suggest that 97% of the samples carry the most prevalent invader genotype already reported, while the rest shows a close mitochondrial derivative. This would support the hypothesis of a general purpose genotype, with parthenogenesis and its associated lack of recombination maintaining the linkage of genetic variants capable of coping with adverse conditions and enlarging its geographical range. However, demographic advantages related to parthenogenetic reproduction as the main driver of geographic expansion (such as the foundation of a population with a single virgin female) cannot be ruled out. Given the historical introduction records and the prevalence of the invader genotype, it is possible that the continental US may act as a secondary source of introductions to other areas. We propose that both the parthenogenesis and scarce genetic variation in places of introduction may, in fact, be an asset that allows N. cervinus to thrive across a range of environmental conditions.

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

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.

Recurrent SMARCB1 Mutations Reveal a Nucleosome Acidic Patch Interaction Site That Potentiates mSWI/SNF Complex Chromatin Remodeling.

Mammalian switch/sucrose non-fermentable (mSWI/SNF) complexes are multi-component machines that remodel chromatin architecture. Dissection of the subunit- and domain-specific contributions to complex activities is needed to advance mechanistic understanding. Here, we examine the molecular, structural, and genome-wide regulatory consequences of recurrent, single-residue mutations in the putative coiled-coil C-terminal domain (CTD) of the SMARCB1 (BAF47) subunit, which cause the intellectual disability disorder Coffin-Siris syndrome (CSS), and are recurrently found in cancers. We find that the SMARCB1 CTD contains a basic α helix that binds directly to the nucleosome acidic patch and that all CSS-associated mutations disrupt this binding. Furthermore, these mutations abrogate mSWI/SNF-mediated nucleosome remodeling activity and enhancer DNA accessibility without changes in genome-wide complex localization. Finally, heterozygous CSS-associated SMARCB1 mutations result in dominant gene regulatory and morphologic changes during iPSC-neuronal differentiation. These studies unmask an evolutionarily conserved structural role for the SMARCB1 CTD that is perturbed in human disease.