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Research Article

Evolutionary dynamics of recent selection on cognitive abilities

View ORCID ProfileSara E. Miller, Andrew W. Legan, Michael T. Henshaw, Katherine L. Ostevik, View ORCID ProfileKieran Samuk, Floria M. K. Uy, and View ORCID ProfileMichael J. Sheehan
PNAS first published January 24, 2020 https://doi.org/10.1073/pnas.1918592117
Sara E. Miller
aDepartment of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853;
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Andrew W. Legan
aDepartment of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853;
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Michael T. Henshaw
bDepartment of Biology, Grand Valley State University, Allendale, MI 49401;
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Katherine L. Ostevik
cDepartment of Biology, Duke University, Durham, NC 27708;
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Kieran Samuk
cDepartment of Biology, Duke University, Durham, NC 27708;
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Floria M. K. Uy
aDepartment of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853;dDepartment of Biology, University of Miami, Coral Gables, FL 33146
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Michael J. Sheehan
aDepartment of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853;
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  • ORCID record for Michael J. Sheehan
  • For correspondence: msheehan@cornell.edu
  1. Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved December 29, 2019 (received for review November 2, 2019)

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Significance

Humans have long been fascinated by animal cognition, but little research has addressed the dynamics of the evolution of cognitive traits. Does cognitive evolution involve strong selection on novel mutations or selection on preexisting genetic variation? Do selective events happen in concert or in multiple independent bouts? We examined population genomic signatures of cognitive adaptation in Polistes fuscatus paper wasps, which have recently evolved individual facial recognition. We find evidence for multiple hard selective sweeps of novel mutations associated with genes involved in learning, memory, brain development, and visual processing. Arguably, selection on cognition has been among the strongest selective pressures in the species’ recent history. These data provide insight into the evolutionary processes by which new cognitive traits evolve.

Abstract

Cognitive abilities can vary dramatically among species. The relative importance of social and ecological challenges in shaping cognitive evolution has been the subject of a long-running and recently renewed debate, but little work has sought to understand the selective dynamics underlying the evolution of cognitive abilities. Here, we investigate recent selection related to cognition in the paper wasp Polistes fuscatus—a wasp that has uniquely evolved visual individual recognition abilities. We generate high quality de novo genome assemblies and population genomic resources for multiple species of paper wasps and use a population genomic framework to interrogate the probable mode and tempo of cognitive evolution. Recent, strong, hard selective sweeps in P. fuscatus contain loci annotated with functions in long-term memory formation, mushroom body development, and visual processing, traits which have recently evolved in association with individual recognition. The homologous pathways are not under selection in closely related wasps that lack individual recognition. Indeed, the prevalence of candidate cognition loci within the strongest selective sweeps suggests that the evolution of cognitive abilities has been among the strongest selection pressures in P. fuscatus’ recent evolutionary history. Detailed analyses of selective sweeps containing candidate cognition loci reveal multiple cases of hard selective sweeps within the last few thousand years on de novo mutations, mainly in noncoding regions. These data provide unprecedented insight into some of the processes by which cognition evolves.

  • cognition
  • selective sweeps
  • evolutionary dynamics
  • wasps
  • social evolution

Footnotes

  • ↵1To whom correspondence may be addressed. Email: msheehan{at}cornell.edu.
  • Author contributions: S.E.M. and M.J.S. designed research; S.E.M., A.W.L., M.T.H., K.L.O., K.S., F.M.K.U., and M.J.S. performed research; S.E.M. and M.J.S. analyzed data; and S.E.M. and M.J.S. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Sequence data are available at the National Center for Biotechnology Information (NCBI) Sequence Read Archive, https://www.ncbi.nlm.nih.gov/sra (Bioproject accession no. PRJNA482994).

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1918592117/-/DCSupplemental.

Published under the PNAS license.

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Evolutionary dynamics of recent selection on cognitive abilities
Sara E. Miller, Andrew W. Legan, Michael T. Henshaw, Katherine L. Ostevik, Kieran Samuk, Floria M. K. Uy, Michael J. Sheehan
Proceedings of the National Academy of Sciences Jan 2020, 201918592; DOI: 10.1073/pnas.1918592117

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Evolutionary dynamics of recent selection on cognitive abilities
Sara E. Miller, Andrew W. Legan, Michael T. Henshaw, Katherine L. Ostevik, Kieran Samuk, Floria M. K. Uy, Michael J. Sheehan
Proceedings of the National Academy of Sciences Jan 2020, 201918592; DOI: 10.1073/pnas.1918592117
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Article Classifications

  • Biological Sciences
  • Evolution

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  • Article
    • Abstract
    • De Novo Assembly of Three High Quality Polistes Wasp Genomes
    • Recent Strong Selection on Visual Cognition, Neural, and Learning and Memory Annotated Loci in P. fuscatus
    • Recent Extreme Selection on Cognition Loci Is Specific to P. fuscatus
    • Evidence for Multiple Hard Sweeps of De Novo Mutations Associated with Cognitive Evolution
    • The Strongest Signatures of Selection on Cognition in P. fuscatus Are Predominantly Noncoding
    • Timing of Selective Events
    • Mode and Tempo of Cognitive Evolution
    • Materials and Methods
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