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Molodtsova D, Harpur BA, Kent CF, et al. Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors. Front Genet. 2014;5:431doi: 10.3389/fgene.2014.00431.
Molodtsova, D., Harpur, B. A., Kent, C. F., Seevananthan, K., & Zayed, A. (2014). Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors. Frontiers in genetics, 5431. https://doi.org/10.3389/fgene.2014.00431
Molodtsova, Daria, et al. "Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors." Frontiers in genetics vol. 5 (2014): 431. doi: https://doi.org/10.3389/fgene.2014.00431
Molodtsova D, Harpur BA, Kent CF, Seevananthan K, Zayed A. Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors. Front Genet. 2014 Dec 23;5:431. doi: 10.3389/fgene.2014.00431. eCollection 2014. PMID: 25566318; PMCID: PMC4275039.
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Front Genet. 2014 Dec 23;5:431. doi: 10.3389/fgene.2014.00431. eCollection 2014.

Pleiotropy constrains the evolution of protein but not regulatory sequences in a transcription regulatory network influencing complex social behaviors.

Frontiers in genetics

Daria Molodtsova, Brock A Harpur, Clement F Kent, Kajendra Seevananthan, Amro Zayed

Affiliations

  1. Department of Biology, York University Toronto, ON, Canada.
  2. Department of Computer Science and Engineering, York University Toronto, ON, Canada.

PMID: 25566318 PMCID: PMC4275039 DOI: 10.3389/fgene.2014.00431

Abstract

It is increasingly apparent that genes and networks that influence complex behavior are evolutionary conserved, which is paradoxical considering that behavior is labile over evolutionary timescales. How does adaptive change in behavior arise if behavior is controlled by conserved, pleiotropic, and likely evolutionary constrained genes? Pleiotropy and connectedness are known to constrain the general rate of protein evolution, prompting some to suggest that the evolution of complex traits, including behavior, is fuelled by regulatory sequence evolution. However, we seldom have data on the strength of selection on mutations in coding and regulatory sequences, and this hinders our ability to study how pleiotropy influences coding and regulatory sequence evolution. Here we use population genomics to estimate the strength of selection on coding and regulatory mutations for a transcriptional regulatory network that influences complex behavior of honey bees. We found that replacement mutations in highly connected transcription factors and target genes experience significantly stronger negative selection relative to weakly connected transcription factors and targets. Adaptively evolving proteins were significantly more likely to reside at the periphery of the regulatory network, while proteins with signs of negative selection were near the core of the network. Interestingly, connectedness and network structure had minimal influence on the strength of selection on putative regulatory sequences for both transcription factors and their targets. Our study indicates that adaptive evolution of complex behavior can arise because of positive selection on protein-coding mutations in peripheral genes, and on regulatory sequence mutations in both transcription factors and their targets throughout the network.

Keywords: Apis mellifera; evo devo; natural selection; network hubs; social evolution

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