Large-Scale Coding Sequence Change Underlies the Evolution of Postdevelopmental Novelty in Honey Bees

Jasper, W. Cameron; Linksvayer, Timothy A.; Atallah, Joel; Friedman, Daniel; Chiu, Joanna C.; Johnson, Brian R.

doi:10.1093/molbev/msw022

Cited by 25 publications

(46 citation statements)

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“…Our study lends support to the notion that social traits may have distinct genetic and evolutionary features (Mikheyev and Linksvayer 2015), even though the evolution of complex social traits such as caste is mainly based on the recruitment of ancient genes. Our results thus help to tie together previous sociogenomic studies, which have largely been motivated by concepts from Evolutionary Developmental Biology (Toth and Robinson 2007) and have stressed the importance of either highly conserved (Toth and Robinson 2007; Woodard et al 2011; O’Connell and Hofmann 2012; Berens et al 2015) or novel genes (Johnson and Tsutsui 2011; Ferreira et al 2013; Feldmeyer et al 2014; Sumner 2014; Jasper et al 2016), with population genetic models based on well-established social evolution theory (Hamilton 1964; Linksvayer and Wade 2009, 2016; Hall and Goodisman 2012). …”

supporting

confidence: 59%

Genomic Signature of Kin Selection in an Ant with Obligately Sterile Workers

Warner

Mikheyev

Linksvayer

2017

Molecular Biology and Evolution

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Kin selection is thought to drive the evolution of cooperation and conflict, but the specific genes and genome-wide patterns shaped by kin selection are unknown. We identified thousands of genes associated with the sterile ant worker caste, the archetype of an altruistic phenotype shaped by kin selection, and then used population and comparative genomic approaches to study patterns of molecular evolution at these genes. Consistent with population genetic theoretical predictions, worker-upregulated genes experienced reduced selection compared with genes upregulated in reproductive castes. Worker-upregulated genes included more taxonomically restricted genes, indicating that the worker caste has recruited more novel genes, yet these genes also experienced reduced selection. Our study identifies a putative genomic signature of kin selection and helps to integrate emerging sociogenomic data with longstanding social evolution theory.

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supporting

confidence: 59%

Genomic Signature of Kin Selection in an Ant with Obligately Sterile Workers

Warner

Mikheyev

Linksvayer

2017

Molecular Biology and Evolution

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“…; Sumner ; Jasper et al. ). This study provides further insight on the role of new genes, created through the process of gene duplication, in the evolution of insect societies.…”

Section: Discussionmentioning

confidence: 99%

“…; Jasper et al. ). Tau ranges from 0 to 1 with low values indicating that a gene is broadly expressed among tissues and high values indicating that a gene is expressed in few tissues.…”

Section: Methodsmentioning

confidence: 96%

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Gene duplication and the evolution of phenotypic diversity in insect societies

Chau

Goodisman

2017

Evolution

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Gene duplication is an important evolutionary process thought to facilitate the evolution of phenotypic diversity. We investigated if gene duplication was associated with the evolution of phenotypic differences in a highly social insect, the honeybee Apis mellifera. We hypothesized that the genetic redundancy provided by gene duplication could promote the evolution of social and sexual phenotypes associated with advanced societies. We found a positive correlation between sociality and rate of gene duplications across the Apoidea, indicating that gene duplication may be associated with sociality. We also discovered that genes showing biased expression between A. mellifera alternative phenotypes tended to be found more frequently than expected among duplicated genes than singletons. Moreover, duplicated genes had higher levels of caste-, sex-, behavior-, and tissue-biased expression compared to singletons, as expected if gene duplication facilitated phenotypic differentiation. We also found that duplicated genes were maintained in the A. mellifera genome through the processes of conservation, neofunctionalization, and specialization, but not subfunctionalization. Overall, we conclude that gene duplication may have facilitated the evolution of social and sexual phenotypes, as well as tissue differentiation. Thus this study further supports the idea that gene duplication allows species to evolve an increased range of phenotypic diversity.

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“…), and as such has emerged as a preeminent model for social gene discovery (e.g., Zayed and Robinson ; Jasper et al. ; Mullen and Thompson ). Early screens have yielded hundreds of genes associated in their transmission or their expression with honeybee social traits, including genes associated with queen–worker caste differentiation (Evans and Wheeler ; Barchuk et al.…”

Section: Introductionmentioning

confidence: 99%

Structure and function of gene regulatory networks associated with worker sterility in honeybees

Sobotka

Daley

Chandrasekaran

et al. 2016

Ecology and Evolution

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A characteristic of eusocial bees is a reproductive division of labor in which one or a few queens monopolize reproduction, while her worker daughters take on reproductively altruistic roles within the colony. The evolution of worker reproductive altruism involves indirect selection for the coordinated expression of genes that regulate personal reproduction, but evidence for this type of selection remains elusive. In this study, we tested whether genes coexpressed under queen‐induced worker sterility show evidence of adaptive organization within a model brain transcriptional regulatory network (TRN). If so, this structured pattern would imply that indirect selection on nonreproductive workers has influenced the functional organization of genes within the network, specifically to regulate the expression of sterility. We found that literature‐curated sets of candidate genes for sterility, ranging in size from 18 to 267, show strong evidence of clustering within the three‐dimensional space of the TRN. This finding suggests that our candidate sets of genes for sterility form functional modules within the living bee brain's TRN. Moreover, these same gene sets colocate to a single, albeit large, region of the TRN's topology. This spatially organized and convergent pattern contrasts with a null expectation for functionally unrelated genes to be haphazardly distributed throughout the network. Our meta‐genomic analysis therefore provides first evidence for a truly “social transcriptome” that may regulate the conditional expression of honeybee worker sterility.

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Large-Scale Coding Sequence Change Underlies the Evolution of Postdevelopmental Novelty in Honey Bees

Cited by 25 publications

References 0 publications

Genomic Signature of Kin Selection in an Ant with Obligately Sterile Workers

Genomic Signature of Kin Selection in an Ant with Obligately Sterile Workers

Gene duplication and the evolution of phenotypic diversity in insect societies

Structure and function of gene regulatory networks associated with worker sterility in honeybees

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