Decoupled maternal and zygotic genetic effects shape the evolution of development

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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.

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

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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.
Jennifer M Deutscher

Department of Biology, New York University, New York, United States

Competing interests
The authors declare that no competing interests exist.
Alex D Kay

Department of Biology, New York University, New York, United States

Competing interests
The authors declare that no competing interests exist.
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.

"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.

Copyright

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.