The evolution of cell types in animals: emerging principles from molecular studies (original) (raw)
Leys, S. P. & Degnan, B. M. Cytological basis of photoresponsive behavior in a sponge larva. Biol. Bull.201, 323–338 (2001). ArticleCASPubMed Google Scholar
Vickaryous, M. K. & Hall, B. K. Human cell type diversity, evolution, development, and classification with special reference to cells derived from the neural crest. Biol. Rev. Camb. Philos. Soc.81, 425–455 (2006). ArticlePubMed Google Scholar
Valentine, J. W. in Keywords and Concepts in Evolutionary Devlopmental Biology (eds Hall, B. K. & Olson, W. M.) 35–53 (Harvard Univ. Press, Cambridge, 2003). Google Scholar
Arendt, D. Evolution of eyes and photoreceptor cell types. Int. J. Dev. Biol.47, 563–571 (2003). PubMed Google Scholar
Willmer, E. N. Cytology and Evolution (Academic Press, New York and London, 1970). Google Scholar
Salvini-Plawen, L. V. & Mayr, E. in Evolutionary Biology Vol. 10 (eds Hecht, M. K., Steere, W. C. & Wallace, B.) 207–263 (Plenum, New York, 1977). Book Google Scholar
Arendt, D., Tessmar-Raible, K., Snyman, H., Dorresteijn, A. W. & Wittbrodt, J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science306, 869–871 (2004). ArticleCASPubMed Google Scholar
Royuela, M., Fraile, B., Arenas, M. I. & Paniagua, R. Characterization of several invertebrate muscle cell types: a comparison with vertebrate muscles. Microsc. Res. Tech.48, 107–115 (2000). ArticleCASPubMed Google Scholar
Seipel, K. & Schmid, V. Evolution of striated muscle: jellyfish and the origin of triploblasty. Dev. Biol.282, 14–26 (2005). ArticleCASPubMed Google Scholar
Arendt, D. Genes and homology in nervous system evolution: comparing gene functions, expression patterns, and cell type molecular fingerprints. Theory Biosci.124, 185–197 (2005). A conceptual review that discusses the different levels of homology in evolutionary developmental biology research; it introduces the concept of molecular fingerprints for cell type comparisons. ArticleCASPubMed Google Scholar
Seipel, K., Yanze, N. & Schmid, V. Developmental and evolutionary aspects of the basic helix–loop–helix transcription factors Atonal-like 1 and Achaete-scute homolog 2 in the jellyfish. Dev. Biol.269, 331–345 (2004). ArticleCASPubMed Google Scholar
Tessmar-Raible, K. et al. Conserved sensory–neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell129, 1389–1400 (2007). This paper unravels striking similarities in the regional specification and cell type inventory of the developing brain neurosecretory system in annelids and vertebrates. ArticleCASPubMed Google Scholar
Putnam, N. H. et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science317, 86–94 (2007). ArticleCASPubMed Google Scholar
Lee, S. K. & Pfaff, S. L. Transcriptional networks regulating neuronal identity in the developing spinal cord. Nature Neurosci.4, S1183–S1191 (2001). Article Google Scholar
Wienholds, E. et al. MicroRNA expression in zebrafish embryonic development. Science309, 310–311 (2005). ArticleCASPubMed Google Scholar
Raible, F. et al. Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science310, 1325–1326 (2005). ArticleCASPubMed Google Scholar
Kortschak, R. D., Samuel, G., Saint, R. & Miller, D. J. EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates. Curr. Biol.13, 2190–2195 (2003). ArticleCASPubMed Google Scholar
Koyanagi, M., Terakita, A., Kubokawa, K. & Shichida, Y. Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-_cis_- and all-_trans_-retinals as their chromophores. FEBS Lett.531, 525–528 (2002). ArticleCASPubMed Google Scholar
Altincicek, B. & Vilcinskas, A. Analysis of the immune-related transcriptome of a lophotrochozoan model, the marine annelid Platynereis dumerilii. Front. Zool.4, 18 (2007). ArticlePubMedPubMed CentralCAS Google Scholar
Thor, S. & Thomas, J. Motor neuron specification in worms, flies and mice: conserved and 'lost' mechanisms. Curr. Opin. Genet. Dev.12, 558–564 (2002). ArticleCASPubMed Google Scholar
Denes, A. S. et al. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell129, 277–288 (2007). ArticleCASPubMed Google Scholar
Rusten, T. E., Cantera, R., Kafatos, F. C. & Barrio, R. The role of TGFβ signaling in the formation of the dorsal nervous system is conserved between Drosophila and chordates. Development129, 3575–3584 (2002). ArticleCASPubMed Google Scholar
Dufour, H. D. et al. Precraniate origin of cranial motoneurons. Proc. Natl Acad. Sci. USA103, 8727–8732 (2006). A pioneering study that elucidates the homology between motor neurons in the brain of adult ascidians and in the hindbrain of vertebrates, exemplifying the cell type comparative approach. ArticleCASPubMedPubMed Central Google Scholar
Isoldi, M. C., Rollag, M. D., Castrucci, A. M. & Provencio, I. Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin. Proc. Natl Acad. Sci. USA102, 1217–1221 (2005). ArticleCASPubMedPubMed Central Google Scholar
Koyanagi, M., Kubokawa, K., Tsukamoto, H., Shichida, Y. & Terakita, A. Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr. Biol.15, 1065–1069 (2005). ArticleCASPubMed Google Scholar
Plachetzki, D. C., Degnan, B. M. & Oakley, T. H. The origins of novel protein interactions during animal opsin evolution. PLoS ONE2, e1054 (2007). ArticlePubMedPubMed CentralCAS Google Scholar
Suga, H., Schmid, V. & Gehring, W. J. Evolution and functional diversity of jellyfish opsins. Curr. Biol.18, 51–55 (2008). ArticleCASPubMed Google Scholar
Arendt, D., Tessmar, K., de Campos-Baptista, M. I., Dorresteijn, A. & Wittbrodt, J. Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development129, 1143–1154 (2002). ArticleCASPubMed Google Scholar
Velarde, R. A., Sauer, C. D., Walden, K. K., Fahrbach, S. E. & Robertson, H. M. Pteropsin: a vertebrate-like non-visual opsin expressed in the honey bee brain. Insect Biochem. Mol. Biol.35, 1367–1377 (2005). ArticleCASPubMed Google Scholar
Blackshaw, S. & Snyder, S. H. Encephalopsin: a novel mammalian extraretinal opsin discretely localized in the brain. J. Neurosci.19, 3681–3690 (1999). ArticleCASPubMedPubMed Central Google Scholar
Arendt, D. & Wittbrodt, J. Reconstructing the eyes of Urbilateria. Phil. Trans. R. Soc. Lond. Biol. Sci. B356, 1545–1563 (2001). ArticleCAS Google Scholar
Lamb, T. D., Collin, S. P. & Pugh, E. N. Jr. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nature Rev. Neurosci.8, 960–976 (2007). An essential read for those interested in vertebrate eye evolution. The authors discuss the evolution of retinal cell types with a special emphasis on opsins and on bipolar cells. ArticleCAS Google Scholar
Salo, E. et al. Genetic network of the eye in Platyhelminthes: expression and functional analysis of some players during planarian regeneration. Gene287, 67–74 (2002). ArticleCASPubMed Google Scholar
Candiani, S., Holland, N. D., Oliveri, D., Parodi, M. & Pestarino, M. Expression of the amphioxus Pit-1 gene (AmphiPOU1F1/Pit-1) exclusively in the developing preoral organ, a putative homolog of the vertebrate adenohypophysis. Brain Res. Bull.75, 324–330 (2008). ArticleCASPubMed Google Scholar
de Velasco, B. et al. Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. Dev. Biol.302, 309–323 (2007). ArticleCASPubMed Google Scholar
Hartenstein, V. The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. J. Endocrinol.190, 555–570 (2006). A comprehensive review of the anatomy and hormone release of neuroendocrine systems in various invertebrates. It also provides a detailed comparison of neuroendocrine-system specification in vertebrates and insects. ArticleCASPubMed Google Scholar
Tessmar-Raible, K. The evolution of neurosecretory centers in bilaterian forebrains: insights from protostomes. Semin. Cell Dev. Biol.18, 492–501 (2007). ArticleCASPubMed Google Scholar
Lacalli, T. Mucus secretion and transport in amphioxus larvae: organization and ultrastructure of the food trapping system, and implications for head evolution. Acta Zool. Stockholm89, 219–230 (2008). Article Google Scholar
Kozmik, Z. et al. Pax–Six–Eya–Dach network during amphioxus development: conservation in vitro but context specificity in vivo. Dev. Biol.306, 143–159 (2007). ArticleCASPubMed Google Scholar
Welsch, L. T. & Welsch, U. Histologische und elekronmikroskopische Untersuchungen an der präoralen Wimpergrube von Saccoglossus horsti (Hemichordata) und der Hatschekschen Grube von Branchiostoma lanceolatum (Acrania). Ein Beirag zur phylogenetischen Entwicklung der Adenohypophyse. Zool. Jahrb. Anat.100, 564–578 (1978). Google Scholar
Yasui, K., Zhang, S., Uemura, M. & Saiga, H. Left–right asymmetric expression of BbPtx, a Ptx-related gene, in a lancelet species and the developmental left-sidedness in deuterostomes. Development127, 187–195 (2000). ArticleCASPubMed Google Scholar
Nozaki, M. & Gorbman, A. The question of functional homology of Hatschek's pit of amphioxus (Branchiostoma belcheri) and the vertebrate adenohypophysis. Zool. Sci.9, 387–395 (1992). CAS Google Scholar
Hartenstein, V. Blood cells and blood cell development in the animal kingdom. Annu. Rev. Cell Dev. Biol.22, 677–712 (2006). An excellent survey of blood cell types in various bilaterians. Hartenstein speculates on how the diverse cell types of the immune system in extant animals have evolved from common evolutionary precursors. ArticleCASPubMed Google Scholar
Evans, C. J., Hartenstein, V. & Banerjee, U. Thicker than blood: conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev. Cell5, 673–690 (2003). ArticleCASPubMed Google Scholar
Palmer, C., Diehn, M., Alizadeh, A. A. & O'Brown, P. Cell-type specific gene expression profiles of leukocytes in human peripheral blood. BMC Genomics7, 115 (2006). ArticlePubMedPubMed CentralCAS Google Scholar
Li, J. et al. cDNA microarray analysis reveals fundamental differences in the expression profiles of primary human monocytes, monocyte-derived macrophages, and alveolar macrophages. J. Leukoc. Biol.81, 328–335 (2007). ArticleCASPubMed Google Scholar
Franc, N. C., Heitzler, P., Ezekowitz, R. A. & White, K. Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science284, 1991–1994 (1999). ArticleCASPubMed Google Scholar
Fadok, V. A. et al. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature405, 85–90 (2000). ArticleCASPubMed Google Scholar
Pancer, Z. & Cooper, M. D. The evolution of adaptive immunity. Annu. Rev. Immunol.24, 497–518 (2006). ArticleCASPubMed Google Scholar
Pancer, Z. Dynamic expression of multiple scavenger receptor cysteine-rich genes in coelomocytes of the purple sea urchin. Proc. Natl Acad. Sci. USA97, 13156–13161 (2000). ArticleCASPubMedPubMed Central Google Scholar
Smith, L. C., Shih, C. S. & Dachenhausen, S. G. Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J. Immunol.161, 6784–6793 (1998). CASPubMed Google Scholar
Gross, P. S., Clow, L. A. & Smith, L. C. SpC3, the complement homologue from the purple sea urchin, Strongylocentrotus purpuratus, is expressed in two subpopulations of the phagocytic coelomocytes. Immunogenetics51, 1034–1144 (2000). ArticleCASPubMed Google Scholar
Crozatier, M., Ubeda, J. M., Vincent, A. & Meister, M. Cellular immune response to parasitization in Drosophila requires the EBF orthologue collier. PLoS Biol.2, E196 (2004). ArticlePubMedPubMed CentralCAS Google Scholar
Hartenstein, V. & Mandal, L. The blood/vascular system in a phylogenetic perspective. Bioessays28, 1203–1210 (2006). ArticlePubMed Google Scholar
Sugino, K. et al. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nature Neurosci.9, 99–107 (2006). Pioneering work on the classification of neuron types in the vertebrate telencephalon, based on expression profiling. ArticleCASPubMed Google Scholar
Blackshaw, S., Fraioli, R. E., Furukawa, T. & Cepko, C. L. Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes. Cell107, 579–589 (2001). ArticleCASPubMed Google Scholar
Vigh, B. et al. The system of cerebrospinal fluid-contacting neurons. Its supposed role in the nonsynaptic signal transmission of the brain. Histol. Histopathol.19, 607–628 (2004). This is one of the many excellent reviews by Vigh on the system of cerebrospinal fluid-contacting neurons in vertebrates and the supposed evolutionary origin of such neurons from an ancient 'protoneuron'. CASPubMed Google Scholar
Leys, S. P., Cronin, T. W., Degnan, B. M. & Marshall, J. N. Spectral sensitivity in a sponge larva. J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol.188, 199–202 (2002). ArticlePubMed Google Scholar
Nordstrom, K., Wallen, R., Seymour, J. & Nilsson, D. A simple visual system without neurons in jellyfish larvae. Proc. R. Soc. Lond. B270, 2349–2354 (2003). Article Google Scholar
Mackie, G. O. Neuroid conduction and the evolution of conducting tissues. Q. Rev. Biol.45, 319–332 (1970). ArticleCASPubMed Google Scholar
Clark, J. Note on the infusoria flagellata and the spongiae ciliatae. Am. J. Sci.1, 113–114 (1866). Google Scholar
Philippe, H. et al. Phylogenomics of eukaryotes: impact of missing data on large alignments. Mol. Biol. Evol.21, 1740–1752 (2004). ArticleCASPubMed Google Scholar
Lang, B. F., O'Kelly, C., Nerad, T., Gray, M. W. & Burger, G. The closest unicellular relatives of animals. Curr. Biol.12, 1773–1778 (2002). ArticleCASPubMed Google Scholar
Liu, I. S. C. et al. Developmental expression of a novel murine homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron13, 377–393 (1994). ArticleCASPubMed Google Scholar
Chow, R. L. et al. Vsx1, a rapidly evolving paired-like homeobox gene expressed in cone bipolar cells. Mech. Dev.109, 315–322 (2001). ArticleCASPubMed Google Scholar
Livne-bar, I. et al. Chx10 is required to block photoreceptor differentiation but is dispensable for progenitor proliferation in the postnatal retina. Proc. Natl Acad. Sci. USA103, 4988–4993 (2006). ArticleCASPubMedPubMed Central Google Scholar
Dorval, K. M., Bobechko, B. P., Fujieda, H., Chen, S. & Zack, D. J. Chx10 targets a subset of photoreceptor genes. J. Biol. Chem.281, 744–751 (2006). ArticleCASPubMed Google Scholar
Braasch, I., Schartl, M. & Volff, J. N. Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol. Biol.7, 74 (2007). ArticlePubMedPubMed CentralCAS Google Scholar
Kasahara, M., Suzuki, T. & Pasquier, L. D. On the origins of the adaptive immune system: novel insights from invertebrates and cold-blooded vertebrates. Trends Immunol.25, 105–111 (2004). ArticleCASPubMed Google Scholar
Ding, G. et al. Insights into the coupling of duplication events and macroevolution from an age profile of animal transmembrane gene families. PLoS Comput. Biol.2, e102 (2006). ArticlePubMedPubMed CentralCAS Google Scholar
Collin, S. P. & Trezise, A. E. The origins of colour vision in vertebrates. Clin. Exp. Optom.87, 217–223 (2004). ArticlePubMed Google Scholar
Collin, S. P. et al. Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr. Biol.13, R864–R865 (2003). ArticleCASPubMed Google Scholar
Plachetzki, D. C., Serb, J. M. & Oakley, T. H. New insights into the evolutionary history of photoreceptor cells. Trends Ecol. Evol.20, 465–467 (2005). ArticlePubMed Google Scholar
Plachetzki, D. C. & Oakley, T. H. Key transitions during the evolution of animal phototransduction: novelty, ''tree-thinking'', co-option, and co-duplication. Integr. Comp. Biol.47, 759–769 (2007). An account of the excellent conceptual work of Oakley and colleagues on cell type evolution. Cell type is one of many hierarchical levels of character evolution that evolves according to common principles. ArticleCASPubMed Google Scholar
Nordstrom, K., Larsson, T. A. & Larhammar, D. Extensive duplications of phototransduction genes in early vertebrate evolution correlate with block (chromosome) duplications. Genomics83, 852–872 (2004). ArticleCASPubMed Google Scholar
Oakley, T. H., Plachetzki, D. C. & Rivera, A. S. Furcation, field-splitting, and the evolutionary origins of novelty in arthropod photoreceptors. Arthropod Struct. Dev.36, 386–400 (2007). ArticlePubMed Google Scholar
Lynch, M. The frailty of adaptive hypotheses for the origins of organismal complexity. Proc. Natl Acad. Sci. USA104 (Suppl. 1), 8597–8604 (2007). ArticleCASPubMedPubMed Central Google Scholar
Serb, J. M. & Oakley, T. H. Hierarchical phylogenetics as a quantitative analytical framework for evolutionary developmental biology. Bioessays27, 1158–1166 (2005). ArticleCASPubMed Google Scholar
Nuchter, T., Benoit, M., Engel, U., Ozbek, S. & Holstein, T. W. Nanosecond-scale kinetics of nematocyst discharge. Curr. Biol.16, R316–R318 (2006). ArticleCASPubMed Google Scholar
Hwang, J. S. et al. The evolutionary emergence of cell type-specific genes inferred from the gene expression analysis of Hydra. Proc. Natl Acad. Sci. USA104, 14735–14740 (2007). ArticleCASPubMedPubMed Central Google Scholar
Miljkovic-Licina, M., Gauchat, D. & Galliot, B. Neuronal evolution: analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system. Biosystems76, 75–87 (2004). ArticleCASPubMed Google Scholar
Prud'homme, B. et al. Repeated morphological evolution through _cis_-regulatory changes in a pleiotropic gene. Nature440, 1050–1053 (2006). ArticleCASPubMed Google Scholar
Purschke, G., Arendt, D., Hausen, H. & Müller, M. C. M. Photoreceptor cells and eyes in Annelida. Arthropod Struct. Dev.35, 211–230 (2006). ArticlePubMed Google Scholar
Haeckel, E. Die Gastraea-Theorie, die phylogenetische Classification des Thierreiches und die Homologie der Keimblätter. Jena Z. Naturwiss.8, 1–55 (1874). Google Scholar
Tian, H., Schlager, B., Xiao, H. & Sommer, R. J. Wnt signaling induces vulva development in the nematode Pristionchus pacificus. Curr. Biol.18, 142–146 (2008). ArticleCASPubMed Google Scholar
Hudson, C. & Yasuo, H. A signalling relay involving Nodal and Delta ligands acts during secondary notochord induction in Ciona embryos. Development133, 2855–2864 (2006). ArticleCASPubMed Google Scholar
Yasuo, H. & Hudson, C. FGF8/17/18 functions together with FGF9/16/20 during formation of the notochord in Ciona embryos. Dev. Biol.302, 92–103 (2007). ArticleCASPubMed Google Scholar
Smith, J. C. Making mesoderm — upstream and downstream of Xbra. Int. J. Dev. Biol.45, 219–224 (2001). CASPubMed Google Scholar
Penn, B. H., Bergstrom, D. A., Dilworth, F. J., Bengal, E. & Tapscott, S. J. A. MyoD-generated feed-forward circuit temporally patterns gene expression during skeletal muscle differentiation. Genes. Dev.18, 2348–2353 (2004). ArticleCASPubMedPubMed Central Google Scholar
Sandmann, T. et al. A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes. Dev.21, 436–449 (2007). ArticleCASPubMedPubMed Central Google Scholar
Cripps, R. M. & Olson, E. N. Control of cardiac development by an evolutionarily conserved transcriptional network. Dev. Biol.246, 14–28 (2002). ArticleCASPubMed Google Scholar
Oota, S. & Saitou, N. Phylogenetic relationship of muscle tissues deduced from superimposition of gene trees. Mol. Biol. Evol.16, 856–867 (1999). ArticleCASPubMed Google Scholar
Gans, C. & Northcutt, R. G. Neural crest and the origin of vertebrates: a new head. Science220, 268–273 (1983). ArticleCASPubMed Google Scholar
Sauka-Spengler, T., Meulemans, D., Jones, M. & Bronner-Fraser, M. Ancient evolutionary origin of the neural crest gene regulatory network. Dev. Cell13, 405–420 (2007). ArticleCASPubMed Google Scholar
Martinez-Morales, J. R., Henrich, T., Ramialison, M. & Wittbrodt, J. New genes in the evolution of the neural crest differentiation program. Genome Biol.8, R36 (2007). ArticlePubMedPubMed CentralCAS Google Scholar
Rychel, A. L. & Swalla, B. J. Development and evolution of chordate cartilage. J. Exp. Zoolog. B Mol. Dev. Evol.308, 325–335 (2007). ArticleCAS Google Scholar
Couly, G. F., Coltey, P. M. & Le Douarin, N. M. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development117, 409–429 (1993). ArticleCASPubMed Google Scholar
Donoghue, P. C. J. & Sansom, I. J. Origin and early evolution of vertebrate skeletonization. Microsc. Res. Tech.59, 352–372 (2002). An exceptional review on the evolution of skeletal systems in the deuterostomes. ArticlePubMed Google Scholar
Meulemans, D. & Bronner-Fraser, M. Insights from amphioxus into the evolution of vertebrate cartilage. PLoS ONE2, e787 (2007). The authors define a hierarchy of gene regulatory networks that specifies cell types in the neural crest. The conservation of each level of this network hierarchy is investigated in the basal chordate amphioxus. ArticlePubMedPubMed CentralCAS Google Scholar
Gehring, W. J. & Ikeo, K. Pax6: mastering eye morphogenesis and eye evolution. Trends Genet.15, 371–377 (1999). ArticleCASPubMed Google Scholar
Carl, M., Loosli, F. & Wittbrodt, J. Six3 inactivation reveals its essential role for the formation and patterning of the vertebrate eye. Development129, 4057–4063 (2002). ArticleCASPubMed Google Scholar
Manavathi, B. et al. Repression of Six3 by a corepressor regulates rhodopsin expression. Proc. Natl Acad. Sci. USA104, 13128–13133 (2007). ArticleCASPubMedPubMed Central Google Scholar
Tanabe, Y., William, C. & Jessell, T. M. Specification of motor neuron identity by the MNR2 homeodomain protein. Cell95, 67–80 (1998). ArticleCASPubMed Google Scholar
Pattyn, A. et al. Coordinated temporal and spatial control of motor neuron and serotonergic neuron generation from a common pool of CNS progenitors. Genes Dev.17, 729–737 (2003). ArticleCASPubMedPubMed Central Google Scholar
Chen, C. L. et al. Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron49, 365–377 (2006). ArticleCASPubMed Google Scholar
Kramer, I. et al. A role for Runx transcription factor signaling in dorsal root ganglion sensory neuron diversification. Neuron49, 379–393 (2006). ArticleCASPubMed Google Scholar
Marmigere, F. et al. The Runx1/AML1 transcription factor selectively regulates development and survival of TrkA nociceptive sensory neurons. Nature Neurosci.9, 180–187 (2006). ArticleCASPubMed Google Scholar
Bushati, N. & Cohen, S. M. microRNA functions. Annu. Rev. Cell Dev. Biol.23, 175–205 (2007). ArticleCASPubMed Google Scholar
Gorbman, A. Olfactory origins and evolution of the brain-pituitary endocrine system: facts and speculation. Gen. Comp. Endocrinol.97, 171–178 (1995). A review on the comparative anatomy and evolutionary origin of the vertebrate pituitary. The pituitary is deduced from an olfactory precursor structure in vertebrate ancestors. ArticleCASPubMed Google Scholar
Toro, S. & Varga, Z. M. Equivalent progenitor cells in the zebrafish anterior preplacodal field give rise to adenohypophysis, lens, and olfactory placodes. Semin. Cell Dev. Biol.18, 534–542 (2007). ArticlePubMed Google Scholar
Muske, L. E. Evolution of gonadotropin-releasing hormone (GnRH) neuronal systems. Brain Behav. Evol.42, 215–230 (1993). ArticleCASPubMed Google Scholar
Yoon, H., Enquist, L. W. & Dulac, C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell123, 669–682 (2005). ArticleCASPubMed Google Scholar
Hennig, W. Phylogenetic Systematics (Univ. of Illinois Press, Urbana, 1966). Google Scholar
Page, R. D. & Charleston, M. A. From gene to organismal phylogeny: reconciled trees and the gene tree/species tree problem. Mol. Phylogenet. Evol.7, 231–240 (1997). ArticleCASPubMed Google Scholar
Green, P., Hartenstein, A. Y. & Hartenstein, V. The embryonic development of the Drosophila visual system. Cell Tissue Res.273, 583–598 (1993). ArticleCASPubMed Google Scholar
Ruiz, M. S. & Anadon, R. Some considerations on the fine structure of rhabdomeric photoreceptors in the amphioxus, Branchiostoma lanceolatum (Cephalochordata). J. Hirnforsch32, 159–164 (1991). CASPubMed Google Scholar
Leonhardt, H. in Handbuch der mikroskopischen Anatomie des Menschen Vol. 4 (eds Oksche, A. & Vollrath, L.) 177–666 (Springer, Heidelberg, 1980). Google Scholar
Seipel, K. & Schmid, V. Mesodermal anatomies in cnidarian polyps and medusae. Int. J. Dev. Biol.50, 589–599 (2006). ArticlePubMed Google Scholar