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Evolution of Developmental Gene Regulatory Networks in Echinoids

Citation

Erkenbrack, Eric Matthew (2016) Evolution of Developmental Gene Regulatory Networks in Echinoids. Dissertation (Ph.D.), California Institute of Technology. doi:10.7907/Z95X26WZ. http://resolver.caltech.edu/CaltechTHESIS:04262016-110444326

Abstract

Developmental gene regulatory networks (dGRNs) are assemblages of regulatory genes that direct embryonic development of animal body plans and their morpho-logical structures. dGRNs exhibit recursively-wired circuitry that is encoded in the genome and executed during development. Alteration to the regulatory architecture of dGRNs causes variation in developmental programs both during the development of an individual organism and during the evolution of an individual lineage. The ex-planatory power of these networks is best exemplified by the global dGRN directing early development of the euechinoid sea urchin Strongylocentrotus purpuratus. This network consists of numerous regulatory genes engaging in hundreds of genomic regulatory transactions that collectively direct the delineation of early embryonic domains and the specification of cell lineages. Research on closely-related euechi-noid sea urchins, e.g. Lytechinus variegatus and Paracentrotus lividus, has revealed marked conservation of dGRN architecture in echinoid development, suggesting little appreciable alteration has occurred since their divergence in evolution at least 90 million years ago (mya).

We sought to test whether this observation extends to all sea urchins (echinoids) and undertook a systematic analysis of over 50 regulatory genes in the cidaroid sea urchin Eucidaris tribuloides, surveing their regulatory activity and function in a sea urchin that diverged from euechinoid sea urchins at least 268 mya. Our results revealed extensive alterations have occurred to all levels of echinoid dGRN archi-tecture since the cidaroid-euechinoid divergence. Alterations to mesodermal sub-circuits were particularly striking, including functional di˙erences in specification of non-skeletogenic mesenchyme (NSM), skeletogenic mesenchyme (SM), and en-domesodermal segregation. Specification of endomesodermal embryonic domains revealed that, while their underlying network circuitry had clearly diverged, regu-latory states established in pregastrular embryos of these two groups are strikingly similar. Analyses of E. tribuloides specification leading to the estab-lishment of dorsal-ventral (aboral-oral) larval polarity indicated that regulation of regulatory genes expressed in mesodermal embryonic domains had incurred significantly more alterations than those expressed in endodermal and ectodermal domains. Taken together, this study highlights the ability of dGRN architecture to buffer extensive alterations in the evolution and early development of echinoids and adds further support to the notion that alterations can occur at all levels of dGRN architecture and all stages of embryonic development.

Item Type:Thesis (Dissertation (Ph.D.))
Subject Keywords:sea urchin embryogenesis, gene regulatory networks, regulatory states, developmental evolution, cidaroid, Eucidaris tribuloides, euechinoid, echinoid, echinoderm, skeletogenic mesenchyme, non-skeletogenic mesenchyme, ectoderm, oral-aboral axis, dorsal-ventral axis, endoderm, Delta-Notch signaling, Nodal signaling, ancestral state reconstruction, embryonic development
Degree Grantor:California Institute of Technology
Division:Biology and Biological Engineering
Major Option:Biology
Thesis Availability:Public (worldwide access)
Research Advisor(s):
  • Davidson, Eric H.
Thesis Committee:
  • Bronner, Marianne E. (chair)
  • Sternberg, Paul W.
  • Rothenberg, Ellen V.
  • Phillips, Robert B.
  • Peter, Isabelle
Defense Date:7 April 2016
Funders:
Funding AgencyGrant Number
NSF CREATIV1240626
Record Number:CaltechTHESIS:04262016-110444326
Persistent URL:http://resolver.caltech.edu/CaltechTHESIS:04262016-110444326
DOI:10.7907/Z95X26WZ
Related URLs:
URLURL TypeDescription
http://embryos-and-evolution.comAuthorAuthor personal site
http://dx.doi.org/10.1073/pnas.1509845112DOIArticle adapted for ch. 3
http://dx.doi.org/10.1007/s00427-015-0527-yDOIArticle adapted for ch. 4
http://dx.doi.org/10.1101/044149DOIArticle adapted for ch. 5
ORCID:
AuthorORCID
Erkenbrack, Eric Matthew0000-0001-9375-3279
Default Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:9687
Collection:CaltechTHESIS
Deposited By: Eric Erkenbrack
Deposited On:19 May 2016 21:14
Last Modified:18 May 2017 17:27

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