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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 Insects have evolved remarkably complex social systems. Social wasps are particularly noteworthy because they display gradations in social behaviors. Here, we sequence the genomes of two highly diverged Vespula wasps, V. squamosa and V. maculifrons Buysson (Hymenoptera: Vespidae), to gain greater insight into the evolution of sociality. Both V. squamosa and V. maculifrons are social wasps that live in large colonies characterized by distinct queen and worker castes. However, V. squamosa is a facultative social parasite, and V. maculifrons is its frequent host. We found that the genomes of both species were ~200 Mbp in size, similar to the genome sizes of congeneric species. Analyses of gene expression from members of different castes and developmental stages revealed similarities in expression patterns among immature life stages. We also found evidence of DNA methylation within the genome of both species by directly analyzing DNA sequence reads. Moreover, genes that were highly and uniformly expressed were also relatively highly methylated. We further uncovered evidence of differences in patterns of molecular evolution in the two taxa, consistent with V. squamosa exhibiting alterations in evolutionary pressures associated with its facultatively parasitic or polygyne life history. Finally, rates of gene evolution were correlated with variation in gene expression between castes and developmental stages, as expected if more highly expressed genes were subject to stronger levels of selection. Overall, this study expands our understanding of how social behavior relates to genome evolution in insects. 

Abstract Many lizard species face extinction due to worldwide climate change. The Guatemalan Beaded Lizard, Heloderma charlesbogerti, is a member of the Family Helodermatidae that may be particularly imperiled; fewer than 600 mature individuals are believed to persist in the wild. In addition, H. charlesbogerti lizards are phenotypically remarkable. They are large in size, charismatically patterned, and possess a venomous bite. Here, we report the draft genome of the Guatemalan Beaded Lizard using DNA from a wild-caught individual. The assembled genome totals 2.31 Gb in length, similar in size to the genomes of related species. Single-copy orthologs were used to produce a novel molecular phylogeny, revealing that the Guatemalan Beaded Lizard falls into a clade with the Asian Glass Lizard (Anguidae) and in close association with the Komodo Dragon (Varanidae) and the Chinese Crocodile Lizard (Shinisauridae). In addition, we identified 31,411 protein-coding genes within the genome. Of the genes identified, we found 504 that evolved with a differential constraint on the branch leading to the Guatemalan Beaded Lizard. Lastly, we identified a decline in the effective population size of the Guatemalan Beaded Lizard approximately 400,000 years ago, followed by a stabilization before starting to dwindle again 60,000 years ago. The results presented here provide important information regarding a highly endangered, venomous reptile that can be used in future conservation, functional genetic, and phylogenetic analyses. 

Abstract Many social species show variation in their social structure in response to different environmental conditions. For example, colonies of the yellowjacket waspVespula squamosaare typically headed by a single reproductive queen and survive for only a single season. However, in warmer climates,V. squamosacolonies sometimes persist for multiple years and can grow to extremely large size. We used genetic markers to understand patterns of reproduction and recruitment within these perennial colonies. We genotypedV. squamosaworkers, pre‐reproductive queens, and males from perennial colonies in the southeastern United States at 10 polymorphic microsatellite loci and one mitochondrial DNA locus. We found thatV. squamosafrom perennial nests were produced by multiple reproductives, in contrast to typical annual colonies. Relatedness of nestmates from perennial colonies was significantly lower than relatedness of nestmates from annual colonies. Our analyses of mitochondrial DNA indicated that mostV. squamosaperennial colonies represented semiclosed systems whereby all individuals belonged to a single matriline despite the presence of multiple reproductive females. However, new queens recruited into perennial colonies apparently mated with non‐nestmate males. Notably, perennial and annual colonies did not show significant genetic differences, supporting the hypothesis that perennial colony formation represents an instance of social plasticity. Overall, our results indicate that perennialV. squamosacolonies show substantial changes to their social biology compared to typical annual colonies and demonstrate variation in social behaviors in highly social species. 

Females of many species are polyandrous. However, polyandry can give rise to conflict among individuals within families. We examined the level of polyandry and paternity skew in the common eastern yellowjacket wasp,Vespula maculifrons, in order to gain a greater understanding of conflict in social insects. We collected 10 colonies ofV. maculifronsand genotyped workers and prereproductive queens at highly variable microsatellite markers to assign each to a patriline. Genotypic data revealed evidence of significant paternity skew among patrilines. In addition, we found that patrilines contributed differentially to caste production (worker vs. queen), suggesting an important role for reproductive conflict not previously discovered. We also investigated if patterns of paternity skew and mate number varied over time. However, we found no evidence of changes in levels of polyandry when compared to historical data dating back almost 40 years. Finally, we measured a suite of morphological traits in individuals from the most common and least common patrilines in each colony to test if males that showed highly skewed reproductive success also produced offspring that differed in phenotype. Our data revealed weak correlation between paternity skew and morphological phenotype of offspring sired by different males, suggesting no evidence of evolutionary tradeoffs at the level investigated. Overall, this study is the first to report significant paternity and caste‐associated skew inV. maculifrons, and to investigate the phenotypic consequences of skew in a social wasp. Our results suggest that polyandry can have important consequences on the genetic and social structure of insect societies. 

Eusociality represents an extreme form of social behavior characterized by a reproductive division of labor. Eusociality necessarily evolved through kin selection, which requires interactions among related individuals. However, many eusocial taxa also show cooperation between non-kin groups, challenging the idea that cooperative actions should only occur among relatives. This review explores the causes and consequences of non-kin cooperation in ants. Ants display a diversity of behaviors that lead to non-kin cooperation within and between species. These interactions occur among both reproductive and non-reproductive individuals. The proximate and ultimate mechanisms leading to non-kin cooperative interactions differ substantially depending on the biotic and abiotic environment. We end this review with directions for future research and suggest that the investigation of non-kin cooperative actions provides insight into processes leading to social evolution.