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Evodevo
2013 Oct 07;41:27. doi: 10.1186/2041-9139-4-27.
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Evolution of bilaterian central nervous systems: a single origin?
Holland LZ
,
Carvalho JE
,
Escriva H
,
Laudet V
,
Schubert M
,
Shimeld SM
,
Yu JK
.
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The question of whether the ancestral bilaterian had a central nervous system (CNS) or a diffuse ectodermal nervous system has been hotly debated. Considerable evidence supports the theory that a CNS evolved just once. However, an alternative view proposes that the chordate CNS evolved from the ectodermal nerve net of a hemichordate-like ancestral deuterostome, implying independent evolution of the CNS in chordates and protostomes. To specify morphological divisions along the anterior/posterior axis, this ancestor used gene networks homologous to those patterning three organizing centers in the vertebrate brain: the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer, and subsequent evolution of the vertebrate brain involved elaboration of these ancestral signaling centers; however, all or part of these signaling centers were lost from the CNS of invertebrate chordates. The present review analyzes the evidence for and against these theories. The bulk of the evidence indicates that a CNS evolved just once - in the ancestral bilaterian. Importantly, in both protostomes and deuterostomes, the CNS represents a portion of a generally neurogenic ectoderm that is internalized and receives and integrates inputs from sensory cells in the remainder of the ectoderm. The expression patterns of genes involved in medio/lateral (dorso/ventral) patterning of the CNS are similar in protostomes and chordates; however, these genes are not similarly expressed in the ectoderm outside the CNS. Thus, their expression is a better criterion for CNS homologs than the expression of anterior/posterior patterning genes, many of which (for example, Hox genes) are similarly expressed both in the CNS and in the remainder of the ectoderm in many bilaterians. The evidence leaves hemichordates in an ambiguous position - either CNS centralization was lost to some extent at the base of the hemichordates, or even earlier, at the base of the hemichordates + echinoderms, or one of the two hemichordate nerve cords is homologous to the CNS of protostomes and chordates. In any event, the presence of part of the genetic machinery for the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer in invertebrate chordates together with similar morphology indicates that these organizers were present, at least in part, at the base of the chordates and were probably elaborated upon in the vertebrate lineage.
Figure 1. Four scenarios for evolution of central nervous systems in bilaterians. In scenario 1, the urbilaterian had multiple nerve cords, one of which evolved into the dorsal central nervous system (CNS) of chordates, while another nerve cord evolved into the ventral CNS of protostomes. In scenario 2, the CNSs of protostomes and deuterostomes evolved independently from an ectodermal nerve net in the bilaterian ancestor. In scenario 3, the chordate and protostome nerve cords evolved from a ventral nerve cord in the urbilaterian ancestor. A dorso/ventral (D/V) inversion occurred at the base of the deuterostomes; the dorsal nerve cord of hemichordates is thus homologous to the chordate CNS and to the protostome ventral nerve cord. In scenario 4, the protostome and chordate nerve cords evolved from the CNS of an urbilaterian ancestor, but a D/V inversion occurred at the base of the chordates. Thus, the ventral nerve cord of a hemichordate is homologous to the chordate and protostome CNSs. Scenarios after [1,3,7,23,26-29].
Figure 2. Comparison of metazoan body plans. A typical cnidarian polyp, a generalized protostome, hemichordate and chordate and their phylogenetic relations are shown. Special attention is given to nervous systems and neural structures of the respective animals.
Figure 3. Anterior–posterior gene expression in central nervous systems of three extant bilaterians and the urbilaterian. Anterior–posterior regionalization of gene expression in the central nervous systems of three extant bilaterians (an arthropod, an annelid and a vertebrate) and inferred expression in the last common bilaterian ancestor, the urbilaterian. Expression of Fez and Irx in the annelid Platynereis is unknown. For the urbilaterian, both anterior–posterior and medio-lateral gene expression domains are shown. Hypothetical posterior limits of Irx and Gbx domains in the urbilaterian brain are highlighted by a “?” and dashed lines. PC, protocerebrum; DC, deutocerebrum; TC, tritocerebrum; VC, ventral nerve cord; CG, cerebral ganglion; SG, segmental ganglia; FB, forebrain; MB, midbrain; HB, hindbrain; SC, spinal cord. Gene expression domains based on [1,2,9,24,29,34,42,64],[68-80].
Figure 4. Anterior–posterior gene expression in hemichordate ectoderm and central nervous systems of three chordate subphyla. Anterior–posterior regionalization of gene expression domains in the ectoderm of the hemichordate Saccoglossus kowalevskii as well as in the central nervous system (CNS) of representatives of the three chordate subphyla (that is, amphioxus, ascidian tunicates and vertebrates). Question marks on the diagrams of the amphioxus and ascidian CNS indicate that organizer properties of the regions marked ‘ZLI?’ and ‘ANR?’ have not been tested. AP, anterior proboscis; PB, proboscis; PCB, proboscis/collar boundary; COL, collar; CTB, collar/trunk boundary; TR, trunk; ANR, anterior neural ridge; ZLI, zona limitans intrathalamica; MHB, midbrain/hindbrain boundary; SV, sensory vesicle; N, neck; G, ganglion; ISO, isthmic organizer; Tel, telencephalon; Di, diencephalon; Mes, mesencephalon. Gene expression domains based on [9,24,34,64,68-72,74-80].