Decoupled maternal and zygotic genetic effects shape the evolution of development

  1. Christina Zakas  Is a corresponding author
  2. Jennifer M Deutscher
  3. Alex D Kay
  4. Matthew V Rockman  Is a corresponding author
  1. New York University, United States

Abstract

Evolutionary transitions from indirect to direct development involve changes in both maternal and zygotic genetic factors, with distinctive population-genetic implications, but empirical data on the genetics of such transitions are lacking. The polychaete Streblospio benedicti provides an opportunity to dissect a major transition in developmental mode using forward genetics. Females in this species produce either small eggs that develop into planktonic larvae or large eggs that develop into benthic juveniles. We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. The likely fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.

Data availability

All code and data generated and analyzed during this study can be found in the supplemental files.

Article and author information

Author details

  1. Christina Zakas

    Department of Biology, New York University, New York, United States
    For correspondence
    cz12@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Jennifer M Deutscher

    Department of Biology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Alex D Kay

    Department of Biology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Matthew V Rockman

    Department of Biology, New York University, New York, United States
    For correspondence
    mrockman@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6492-8906

Funding

National Science Foundation (IOS-1350926)

  • Matthew V Rockman

National Institutes of Health (GM108396)

  • Christina Zakas

Zegar Family Foundation

  • Matthew V Rockman

New York University (Biology Master's Research Grant)

  • Alex D Kay

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Magnus Nordborg, Austrian Academy of Sciences, Austria

Version history

  1. Received: March 30, 2018
  2. Accepted: September 9, 2018
  3. Accepted Manuscript published: September 10, 2018 (version 1)
  4. Version of Record published: October 2, 2018 (version 2)

Copyright

© 2018, Zakas et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Christina Zakas
  2. Jennifer M Deutscher
  3. Alex D Kay
  4. Matthew V Rockman
(2018)
Decoupled maternal and zygotic genetic effects shape the evolution of development
eLife 7:e37143.
https://doi.org/10.7554/eLife.37143

Share this article

https://doi.org/10.7554/eLife.37143

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