Gene duplication, co-option and recruitment during the origin of the vertebrate brain from the invertebrate chordate brain

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Brain Behav Evol 2008;72:91–105
DOI: 10.1159/000151470
Gene Duplication, Co-Option and Recruitment
during the Origin of the Vertebrate Brain from the
Invertebrate Chordate Brain
Linda Z. Holland Stephen Short
Marine Biology Research Division, Scripps Institution of Oceanography, University of California at San Diego,
La Jolla,Calif. , USA
tained. Although some genes apparently acquired roles in
neural crest prior to these genome duplications, other key
genes (e.g., FoxD3 in neural crest and Wnt1 at the MHB) were
recruited into the respective gene networks after one or
both genome duplications, suggesting that such an expansion
of the genetic toolkit was critical for the evolution of
these structures. The toolkithas also increased by alternative
splicing. Contrary to the general rule, for at least one gene
family with key roles in neural crest and the MHB, namely Pax
genes, alternative splicing has not decreased subsequent to
gene duplication. Thus, vertebrates have a much larger number
of proteins available for mediating new functions in
these tissues. The creation of new splice forms typicallychanges protein structure more than evolution of the protein
after gene duplication. The functions of particular isoforms
of key proteins expressed at the MHB and in neural
crest have only just begun to be studied. Their roles in modulating
gene networks may turn out to rival gene duplication
for facilitating the evolution of structures such as neural
crest and the MHB. Copyright © 2008 S.Karger AG, Basel
Introduction
Biologists have long been interested in the evolutionary
origin of the vertebrates generally, and, more particularly,
in the origin of vertebrate nervous systems from
Key Words
Lancelet  Neural crest  Midbrain/hindbrain boundary 
MHB  Amphioxus  Tunicate  Alternative splicing 
Genome duplication
Abstract
The brain of the basal chordate amphioxus hasbeen compared
to the vertebrate diencephalic forebrain, midbrain,
hindbrain and spinal cord on the basis of the cell architecture
from serial electron micrographs and patterns of developmental
gene expression. In addition, genes specifying the
neural plate and neural plate border as well as Gbx and Otx ,
that position the midbrain/hindbrain boundary (MHB), are
expressed in comparable patternsin amphioxus and vertebrates.
However, migratory neural crest is lacking in amphioxus,
and although it has homologs of the genes that specify
neural crest, they are not expressed at the edges of the
amphioxus neural plate. Similarly, amphioxus has the genes
that specify organizer properties of the MHB, but they are
not expressed at the Gbx / Otx boundary as in vertebrates.
Thus, the geneticmachinery that created migratory neural
crest and an MHB organizer was present in the ancestral
chordate, but only co-opted for these new roles in vertebrates.
Analyses with the amphioxus genome project strongly
support the idea of two rounds of whole genome duplication
with subsequent gene losses in the vertebrate lineage.
Duplicates of developmental genes were preferentially re-Published online: October 7, 2008
Linda Z. Holland
Marine Biology Research Division
Scripps Institution of Oceanography, University of California San Diego
La Jolla, CA 92093-0202 (USA)
Tel. +01 858 534 5607, Fax +01 858 534 7313, E-Mail lzholland@ucsd.edu
© 2008 S. Karger AG, Basel
Accessible online at:
www.karger.com/bbe
Holland/Short
Brain B 92 ehav Evol 2008;72:91–105
some ancestral nervoussystem in an invertebrate. During
the last two centuries, numerous invertebrate phyla
have been proposed as the proximate ancestors of the vertebrates
[reviewed in Gee, 1996]. Recent molecular phylogenetic
analyses place amphioxus basal in the chordates
and tunicates as the sister group of vertebrates. Even so,
it is now generally agreed that tunicates are quite divergent
and that the...