4.8 Article

Brain diversity evolves via differences in patterning

出版社

NATL ACAD SCIENCES
DOI: 10.1073/pnas.1000395107

关键词

cichlid; development; evolution; forebrain; WNT signaling

资金

  1. National Science Foundation [IOS 0546423, IOS 0922964]
  2. National Institutes of Health [DE017182]
  3. Alfred P. Sloan Foundation [BR4499]
  4. Division Of Integrative Organismal Systems
  5. Direct For Biological Sciences [0922964] Funding Source: National Science Foundation

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Differences in brain region size among species are thought to arise late in development via adaptive control over neurogenesis, as cells of previously patterned compartments proliferate, die, and/or differentiate into neurons. Here we investigate comparative brain development in ecologically distinct cichlid fishes from Lake Malawi and demonstrate that brains vary among recently evolved lineages because of early patterning. Divergence among rock-dwellers and sand-dwellers in the relative size of the telencephalon versus the thalamus is correlated with gene expression variation in a regulatory circuit (composed of six3, fezf2, shh, irx1b, and wnt1) known from model organisms to specify anterior-posterior (AP) brain polarity and position the shh-positive signaling boundary zona limitans intra-thalamica (ZLI) in the forebrain. To confirm that changes in this co-expression network are sufficient to produce the differences we observe, we manipulated WNT signaling in vivo by treating rock-dwelling cichlid embryos with temporally precise doses of LiCl. Chemically treated rock-dwellers develop gene expression patterns, ZLIs, and forebrains distinct from controls and untreated conspecifics, but strongly resembling those of sand-dwellers. Notably, endemic Malawi rock- and sand-dwelling lineages are alternately fixed for an SNP in irx1b, a mediator of WNT signaling required for proper thalamus and ZLI. Together, these natural experiments in neuroanatomy, development, and genomics suggest that evolutionary changes in AP patterning establish ecologically relevant differences in the elaboration of cichlid forebrain compartments. In general, variation in developmental patterning might lay the foundations on which neurogenesis erects diverse brain architectures.

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