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Abstract Supergenes underlying complex trait polymorphisms ensure that sets of coadapted alleles remain genetically linked. Despite their prevalence in nature, the mechanisms of supergene effects on genome regulation are poorly understood. In the fire ant Solenopsis invicta, a supergene containing over 500 individual genes influences trait variation in multiple castes to collectively underpin a colony level social polymorphism. Here, we present results of an integrative investigation of supergene effects on gene regulation. We present analyses of ATAC-seq data to investigate variation in chromatin accessibility by supergene genotype and STARR-seq data to characterize enhancer activity by supergene haplotype. Integration with gene co-expression analyses, newly mapped intact transposable elements (TEs), and previously identified copy number variants (CNVs) collectively reveals widespread effects of the supergene on chromatin structure, gene transcription, and regulatory element activity, with a genome-wide bias for open chromatin and increased expression in the presence of the derived supergene haplotype, particularly in regions that harbor intact TEs. Integrated consideration of CNVs and regulatory element divergence suggests each evolved in concert to shape the expression of supergene encoded factors, including several transcription factors that may directly contribute to the trans-regulatory footprint of a heteromorphic social chromosome. Overall, we show how genome structure in the form of a supergene has wide-reaching effects on gene regulation and gene expression. 

Abstract Characterizing molecular underpinnings of plastic traits and balanced polymorphisms represent 2 important goals of evolutionary biology. Fire ant gynes (pre-reproductive queens) provide an ideal system to study potential links between these phenomena because they exhibit both supergene-mediated polymorphism and nutritional plasticity in weight and colony-founding behaviour. Gynes with the inversion supergene haplotype are lightweight and depend on existing workers to initiate reproduction. Gynes with only the ancestral, non-inverted gene arrangement accumulate more nutrient reserves as adults and, in a distinct colony-founding behaviour, initiate reproduction without help from workers. However, when such gynes overwinter in the natal nest they develop an environmentally induced lightweight phenotype and colony-founding behaviour, similar to gynes with the inversion haplotype that have not overwintered. To evaluate the extent of shared mechanisms between plasticity and balanced polymorphism in fire ant gyne traits, we assessed whether genes with expression variation linked to overwintering plasticity may be affected by the evolutionary divergence between supergene haplotypes. To do so, we first compared transcriptional profiles of brains and ovaries from overwintered and non-overwintered gynes to identify plasticity-associated genes. These genes were enriched for metabolic and behavioural functions. Next, we compared plasticity-associated genes to those differentially expressed by supergene genotype, revealing a significant overlap of the 2 sets in ovarian tissues. We also identified sequence substitutions between supergene variants of multiple plasticity-associated genes, consistent with a scenario in which an ancestrally plastic phenotype responsive to an environmental condition became increasingly genetically regulated. 

Abstract Selfish genetic elements subvert the normal rules of inheritance to unfairly propagate themselves, often at the expense of other genomic elements and the fitness of individuals carrying them. Social life provides diverse avenues for the propagation of such elements. In the fire ant Solenopsis invicta, polymorphic social organization is controlled by a social chromosome, one variant of which (Sb) enhances its own transmission in polygyne colonies through effects on caste development and queen acceptance by workers. Whether the selfish effects of Sb extend to haploid (reproductive) males in this system is less clear. Here, we demonstrate a strong overrepresentation of the Sb social chromosome haplotype in reproductive males, relative to Mendelian expectations, in both the pupal and adult stages. We tested for the presence of selective execution of adult SB males by workers but did not detect such behavior. Combined with the presence of a strong imbalance in the haplotype frequencies already early in the pupal stage, these results indicate that the Sb supergene may distort male haplotype frequencies during larval or embryonic development. These findings are significant because they demonstrate yet another mode by which the selfish tendencies of the Sb supergene are manifested, illuminate complex interactions between Sb and the fire ant breeding system, inform the development of models of the population dynamics of Sb, and illustrate how a selfish supergene can increase in frequency in a population despite harboring deleterious mutations. 

Abstract An ant colony is the epitome of social organization where up to millions of individuals cooperate to survive, compete, and reproduce as a single superorganism, Female members of ant colonies typically are categorized into a reproductive queen caste and a non-reproductive worker caste. The queen(s) conveys her fertility condition and in cases, genotype status, via a suite of queen pheromones whose various functions are crucial to the superorganismal nature of ant colonies. Knowledge of these functional properties is fundamental for identifying constituent chemicals and understanding corresponding modes of actions. In this review, I summarize functional properties of ant queen pheromones learned from seven decades of behavioral experiments, and contextualize this knowledge within the broader understanding of queen pheromones in other major groups of social insects. The effects include promotion of colony integrity and coherence, maintenance of reproductive dominance of the queen, and regulation of colony social structure. Additionally, general characteristics of queen pheromones are discussed and potential avenues for future research are highlighted. 

Abstract The fire antSolenopsis invictaexists in two alternate social forms: monogyne nests contain a single reproductive queen and polygyne nests contain multiple reproductive queens. This colony‐level social polymorphism corresponds with individual differences in queen physiology, queen dispersal patterns and worker discrimination behaviours, all evidently regulated by an inversion‐based supergene that spans more than 13 Mb of a “social chromosome,” contains over 400 protein‐coding genes and rarely undergoes recombination. The specific mechanisms by which this supergene influences expression of the many distinctive features that characterize the alternate forms remain almost wholly unknown. To advance our understanding of these mechanisms, we explore the effects of social chromosome genotype and natal colony social form on gene expression in queens sampled as they embarked on nuptial flights, using RNA‐sequencing of brains and ovaries. We observe a large effect of natal social form, that is, of the social/developmental environment, on gene expression profiles, with similarly substantial effects of genotype, including: (a) supergene‐associated gene upregulation, (b) allele‐specific expression and (c) pronounced extra‐supergenetrans‐regulatory effects. These findings, along with observed spatial variation in differential and allele‐specific expression within the supergene region, highlight the complex gene regulatory landscape that emerged following divergence of the inversion‐mediatedSbhaplotype from its homologue, which presumably largely retained the ancestral gene order. The distinctive supergene‐associated gene expression trajectories we document at the onset of a queen’s reproductive life expand the known record of relevant molecular correlates of a complex social polymorphism and point to putative genetic factors underpinning the alternate social syndromes. 

Abstract Background The tobacco thrips ( Frankliniella fusca Hinds; family Thripidae; order Thysanoptera) is an important pest that can transmit viruses such as the tomato spotted wilt orthotospovirus to numerous economically important agricultural row crops and vegetables. The structural and functional genomics within the order Thysanoptera has only begun to be explored. Within the > 7000 known thysanopteran species, the melon thrips ( Thrips palmi Karny) and the western flower thrips ( Frankliniella occidentalis Pergrande) are the only two thysanopteran species with assembled genomes. Results A genome of F. fusca was assembled by long-read sequencing of DNA from an inbred line. The final assembly size was 370 Mb with a single copy ortholog completeness of ~ 99% with respect to Insecta. The annotated genome of F. fusca was compared with the genome of its congener, F. occidentalis . Results revealed many instances of lineage-specific differences in gene content. Analyses of sequence divergence between the two Frankliniella species’ genomes revealed substitution patterns consistent with positive selection in ~ 5% of the protein-coding genes with 1:1 orthologs. Further, gene content related to its pest status, such as xenobiotic detoxification and response to an ambisense-tripartite RNA virus (orthotospovirus) infection was compared with F. occidentalis . Several F. fusca genes related to virus infection possessed signatures of positive selection. Estimation of CpG depletion, a mutational consequence of DNA methylation, revealed that F. fusca genes that were downregulated and alternatively spliced in response to virus infection were preferentially targeted by DNA methylation. As in many other insects, DNA methylation was enriched in exons in Frankliniella , but gene copies with homology to DNA methyltransferase 3 were numerous and fragmented. This phenomenon seems to be relatively unique to thrips among other insect groups. Conclusions The F. fusca genome assembly provides an important resource for comparative genomic analyses of thysanopterans. This genomic foundation allows for insights into molecular evolution, gene regulation, and loci important to agricultural pest status.