Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

Simola, Daniel F.; Wissler, Lothar; Donahue, Greg; Waterhouse, Robert M.; Helmkampf, Martin; Roux, Julien; Nygaard, Sanne; Glastad, Karl M.; Hagen, Darren E.; Viljakainen, Lumi; Reese, Justin; Hunt, Brendan G.; Graur, Dan; Elhaik, Eran; Kriventseva, Evgenia V.; Wen, Jiayu; Parker, Brian J.; Cash, Elizabeth; Privman, Eyal; Childers, Christopher P.; Muñoz-Torres, Monica; Boomsma, Jacobus J.; Bornberg‐Bauer, Erich; Currie, Cameron R.; Elsik, Christine G.; Suen, Garret; Goodisman, Michael A. D.; Keller, Laurent; Liebig, Jürgen; Rawls, Alan; Reinberg, Danny; Smith, Chris; Smith, Chris R.; Tsutsui, Neil D.; Wurm, Yannick; Zdobnov, Evgeny M.; Berger, Shelley L.; Gadau, Jürgen

doi:10.1101/gr.155408.113

Cited by 224 publications

(281 citation statements)

References 64 publications

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“…Additionally, we uncovered a substantial amount of adaptive regulatory sequence evolution when contrasting differences in allele frequency between the four honey bee lineages studied herein. Our results, along with recent findings of rapid evolution of transcription-factor binding sites in social insects (31), suggests that cis-regulatory changes play an important role in the evolution of insect societies.…”

Section: Discussionsupporting

confidence: 81%

“…Taxonomically restricted genes (TRGs) have been the subject of recent attention because they are predicted to be drivers of phenotypic evolution (30). The genomes of social insects harbor many TRGs, which are hypothesized to play an important role in the elaboration of sociality (31). TRGs in ants (32), bees (33), and wasps (34) tend to show, on average, workerbiased expression, which suggests that they play an important role in the evolution of worker phenotypes.…”

Section: Resultsmentioning

confidence: 99%

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Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Harpur¹,

Kent²,

Molodtsova³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

194

271

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Most theories used to explain the evolution of eusociality rest upon two key assumptions: mutations affecting the phenotype of sterile workers evolve by positive selection if the resulting traits benefit fertile kin, and that worker traits provide the primary mechanism allowing social insects to adapt to their environment. Despite the common view that positive selection drives phenotypic evolution of workers, we know very little about the prevalence of positive selection acting on the genomes of eusocial insects. We mapped the footprints of positive selection in Apis mellifera through analysis of 40 individual genomes, allowing us to identify thousands of genes and regulatory sequences with signatures of adaptive evolution over multiple timescales. We found Apoidea-and Apis-specific genes to be enriched for signatures of positive selection, indicating that novel genes play a disproportionately large role in adaptive evolution of eusocial insects. Worker-biased proteins have higher signatures of adaptive evolution relative to queen-biased proteins, supporting the view that worker traits are key to adaptation. We also found genes regulating worker division of labor to be enriched for signs of positive selection. Finally, genes associated with worker behavior based on analysis of brain gene expression were highly enriched for adaptive protein and cis-regulatory evolution. Our study highlights the significant contribution of worker phenotypes to adaptive evolution in social insects, and provides a wealth of knowledge on the loci that influence fitness in honey bees.natural selection | kin selection | social evolution | taxonomically restricted genes E usocial behavior evolved multiple times in insects and is characterized in part by extreme asymmetries in the reproductive potential of individuals (1). This asymmetry is most pronounced in advanced eusocial insects, with their fertile queen and sterile worker castes. Darwin first recognized that natural selection cannot directly optimize worker phenotypes because workers are usually sterile (2). Hamilton (3, 4) developed kinselection theory to describe the conditions that allow natural selection to indirectly optimize worker phenotypes if such phenotypes benefit their fertile kin. It is commonly believed that worker traits, such as sib-care, foraging, and colony defense, play important roles in allowing colonies to adapt to their environment (5-7). However, despite the central role of kin-selection and inclusive fitness theory in the field of Sociobiology (8, 9), we lack knowledge on the pattern and prevalence of positive selection acting on the genomes of eusocial insects.Population genomic studies provide unprecedented opportunities to detect signatures of selection on DNA sequences over different timescales (10). There are several tests of selection that can be applied to genome-wide datasets. The McDonald-Kreitman (MK) test is arguably the best method for detecting selection on protein coding sequences because of its robustness to changes in a species' demography,...

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Section: Discussionsupporting

confidence: 81%

Section: Resultsmentioning

confidence: 99%

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Harpur¹,

Kent²,

Molodtsova³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

194

271

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“…Relative to other insects, there is a greater number of desaturase genes in ants 62 , although alkenes or polyunsaturated alkenes have not been found in all ants investigated 63 . Z. nevadensis nuttingi displays two alkadienes and two alkatrienes in the cuticular profile of reproductive individuals 49 , but the number of desaturases is at the lower end of the number of putatively functional desaturase genes found in ants (10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23).…”

Section: Discussionmentioning

confidence: 70%

“…Compared with solitary insects there are expansions in number of immunity genes for both Z. nevadensis and ants 62 . However, the expansions occurred in different families, possibly as a result of different selective pressures.…”

Section: Discussionmentioning

confidence: 99%

Molecular traces of alternative social organization in a termite genome

et al. 2014

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Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.

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“…There is a debate over the relative roles for core sets of conserved genes (42-48) and taxon-restricted genes (TRGs) (5,44,47,49,50) in the evolution of convergent phenotypes (7,44,46). We found evidence that both types of gene classes play peripheral roles in the molecular networks associated with phenotypic differentiation in our study species.…”

Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 63%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

200

278

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Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

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Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

Cited by 224 publications

References 64 publications

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits

Molecular traces of alternative social organization in a termite genome

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

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