Serotonin immunoreactive neurons have been studied in an impressive number of arthropod species. Within the framework of this thesis, the list could be supplemented by data for the primary wingless insects Zygentoma and Archaeognatha. As several accounts mentioned variations and inconsistencies in staining intensity even within the same species (e.g., Bishop
and O’Shea, 1983; Longley and Longley, 1986; Radwan et al., 1989; Hörner, 1999; Stemme et al., 2013), I extended the classic method of immunolabeling of serotonin by manipulation using serotonergic drugs, leading to a more detailed picture of the transmitter system.
Serotonin is involved in numerous physiological processes in Arthropoda, acting as neuromodulator and neurohormone (Kravitz, 1988; Bicker and Menzel, 1989). An influence on aggression behavior, locomotion behavior and learning, amongst others has been attributed to this substance (Kravitz, 1988; Bicker and Menzel, 1989). Levels of serotonin can fluctuate due to seasonal (e.g., Catarsi et al., 1990) and circadian rhythms (e.g., Wildt et al., 2004), and thus might be reduced below detection limit of immunolabeling. Nevertheless, for the purpose of phylogenetic considerations it is crucial to identify the complete set of serotonin containing neurons and their major branching pattern. The presented methods are a promising approach to overcome the detection problems and give the opportunity to draw more reliable inferences concerning evolutionary scenarios by the distinction between neuronal serotonin uptake and enzymatic synthesis. At least the ground pattern of Pterygota should be re-investigated with the approach presented here, in order to reconstruct a more detailed pterygote pattern of serotonin containing neurons.
Another important issue, which needs to be resolved in the future, is the situation in the outgroup taxa of Tetraconata. Although several chelicerate and myriapod species have been investigated, the projection patterns of these neurons could not be resolved in detail and the erected ground patterns have to be assessed as preliminary. As a consequence, two contradicting hypotheses are postulated regarding the ground pattern of Tetraconata (see Stegner et al., 2014a and publication 7 in this thesis). However, verification of these hypotheses is substantial for inferences of the evolution of the serotonin transmitter system within Tetraconata and a re-evaluation of outgroup taxa is inevitable. A recent study by Brenneis and Scholtz (2015) revealed that individually identifiable neurons are found in the ventral ganglia of Pycnogonida and suggested them to be part of the ancestral nervous system in arthropods. Medial neurons corresponding to those in Tetraconata are not evident in Pycnogonida. Based on these data, medial neurons would have evolved de nouveau in the lineage of Cephalocarida, Remipedia, and Hexapoda. This feature would be the first synapomorphy of the Miracrustacea, a scenario proposed by Regier et al. (2010; Fig. 1), uniting Remipedia, Cephalocarida and Hexapoda.
The developmental origins of the serotonin immunoreactive neurons have only been unraveled in some pterygote insects (Taghert and Goodman, 1984; Lundell et al., 1996;
Novotny et al., 2002; Karcavich and Doe, 2005). Cell lineage studies of basal insects, crustaceans and other arthropod taxa are still lacking and a putative homology of individually identifiable neurons rely purely on cell body position, neurite morphology, and transmitter phenotype (Kutsch and Breidbach, 1994). Although several developmental studies suggested cellular homologies between arthropod taxa (Thomas et al., 1984; Duman-Scheel and Patel, 1999; Ungerer and Scholtz, 2008) contradictory opinions have been postulated due to considerable divergence in morphological mechanisms in neurogenesis among Arthropoda.
For example, insect neuroblasts delaminate from the ventral neuroectoderm, crustacean neuroblast remain in the ventral-most cell layer (reviewed in Stollewerk 2008, 2016). In conclusion, a direct assignment of homologues between identifiable members of crustacean and insect neural stem cell arrays has so far proven to be elusive and inferences of homology have to be assessed as preliminary.
In summary, the comparison of individually identifiable neurons suggests a close relationship of Remipedia, Cephalocarida, and Hexapoda (Fig. 1). Besides a molecular study by Regier et al. (2010), similar conclusions have been drawn from ovary structure and oogenesis (Kubrakiewicz et al., 2012).
Concluding remarks
This thesis describes the brain anatomy and in particular the structure of the olfactory pathway of certain crustacean species, as well as the distribution and projection pattern of serotonin containing neurons in basal insects for inferring phylogenetic relationships within Tetraconata. Many features of the olfactory pathway have to be interpreted as plesiomorphic.
A clade uniting Malacostraca, Remipedia, and Hexapoda receives certain support.
Interestingly, the comparison of individually identifiable neurons in the ventral nerve cord supports a clade termed Miracrustacea, composed of Cephalocarida, Remipedia, and Hexapoda. The latter hypothesis supports a scenario proposed by Regier et al. (2010).
Although both aspects regarded in this thesis lead to different phylogenetic conclusions – on the one hand a close relationship of Remipedia to Malacostraca and on the other hand to
Cephalocarida – a conspicuous result is the always proposed close affinity to the Hexapoda.
The neuroanatomical data of this thesis provide novel characters for evolutionary analyses and support a growing corpus of literature suggesting Remipedia as a derived taxon within the Tetraconata with close affinities to Hexapoda.
In order to strengthen the phylogenetic inferences drawn from the findings presented in this thesis, certain aspects have to be checked in other taxa. This includes the presence of negative feedback loops in the lateral protocerebrum as well as the occurrence of medial serotonin immunoreactive neurons in the ventral ganglia. This applies especially to the outgroup taxa of Tetraconata, namely the Myriapoda and Chelicerata. While our knowledge on the different tetraconate taxa is successively improving, data on these lineages has remained sparse.
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EFERENCESAndrew DR, Brown SM, Strausfeld NJ. 2012. The minute brain of the copepod Tigriopus californicus supports a complex ancestral ground pattern of the tetraconate cerebral nervous systems. J Comp Neurol 520:3446-3470.
Anton S, Hansson BS. 1996. Antennal lobe interneurons in the desert locust Schistocerca gregaria (Forskal): Processing of aggregation pheromones in adult males and females. J Comp Neurol 370:85-96.
Ax P. 1999. Das System der Metazoa II. Ein Lehrbuch der phylogenetischen Systematik.
Gustav Fischer Verlag, Stuttgart, Jena, Nürnberg, Ulm.
Beltz BS, Kordas K, Lee MM, Long JB, Benton JL, Sandeman D. 2003. Ecological, evolutionary, and functional correlates of sensilla number and glomerular density in the olfactory system of decapod crustaceans. J Comp Neurol 455:260-269.
Beltz BS, Kravitz EA. 1983. Mapping of serotonin-like immunoreactivity in the lobster nervous system. J Neurosci 3:585-602.
Bicker G, Menzel R. 1989. Chemical codes for the control of behaviour in arthropods. Nature 337:33-39.
Bicker G, Schäfer S, Kingan T. 1985. Mushroom body feedback interneurones in the honeybee show GABA-like immunoreactivity. Brain Res 360:394-397.
Bicker G. 1999. Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech 45:174-183.
Bishop CA, O'Shea M. 1983. Serotonin immunoreactive neurons in the central nervous system of an insect (Periplaneta americana). J Neurobiol 14:251-269.
Blaustein DN, Derby CD, Simmons RB, Beall AC. 1988. Structure of the brain and medulla terminalis of the spiny lobster Panulirus argus and the crayfish Procambarus clarkii, with an emphasis on olfactory centers. J Crustacean Biol 8:493-519.
Blenau W, Thamm M. 2011. Distribution of serotonin (5-HT) and its receptors in the insect brain with focus on the mushroom bodies: lessons from Drosophila melanogaster and Apis mellifera. Arthropod Struct Dev 40:381-394.
Boeckh J, Tolbert LP. 1993. Synaptic organization and development of the antennal lobe in insects. Microsc Res Tech 24:260-280.
Böhm A, Szucsich NU, Pass G. 2012. Brain anatomy in Diplura (Hexapoda). Front Zool 9:26.
Brenneis G, Richter S. 2010. Architecture of the nervous system in Mystacocarida (Arthropoda, Crustacea) - an immunohistochemical study and 3D-reconstruction. J Morphol 271:169-189.
Brenneis G, Scholtz G. 2015. Serotonin-immunoreactivity in the ventral nerve cord of Pycnogonida - support for individually identifiable neurons as ancestral feature of the arthropod nervous system. BMC Evol Biol 15:136.
Brenneis G, Stollewerk A, Scholtz G. 2013. Embryonic neurogenesis in Pseudopallene sp.
(Arthropoda, Pycnogonida) includes two subsequent phases with similarities to different arthropod groups. Evodevo 4:32.
Brown S, Wolff G. 2012. Fine structural organization of the hemiellipsoid body of the land hermit crab, Coenobita clypeatus. J Comp Neurol 520:2847-2863.
Callaway JC, Stuart AE. 1999. The distribution of histamine and serotonin in the barnacle's nervous system. Microsc Res Tech 44:94-104.
Catarsi S, Garcia-Gil M, Traina G, Brunelli M. 1990. Seasonal variation of serotonin content and nonassociative learning of swim induction in the leech Hirudo medicinalis. J Comp Physiol A 167:469-474.
Christie AE. 2014. Prediction of the first neuropeptides from a member of the Remipedia (Arthropoda, Crustacea). Gen Comp Endocrinol 201:74-86.
Dacks AM, Christensen TA, Hildebrand JG. 2006. Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 498:727-746.
Dohle W, Scholtz G. 1988. Clonal analysis of the crustacean segment: the discordance between genealogical and segmental borders. Development 104:147-160.
Dohle W. 2001. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name ‘Tetraconata’ for the monophyletic unit Crustacea + Hexapoda. In: Deuve T (ed). Origin of the Hexapoda. Ann Soc Entomol Fr (N S), Vol. 37. pp. 85-103.
Duman-Scheel M, Patel NH. 1999. Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 126:2327-2334.
Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A,
Kristensen RM, Wheeler WC, Martindale MQ, Giribet G. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745-749.
Eickhoff R, Bicker G. 2012. Developmental expression of cell recognition molecules in the mushroom body and antennal lobe of the locust Locusta migratoria. J Comp Neurol 520:2021-2040.
Eisenhardt D, Fiala A, Braun P, Rosenboom H, Kress H, Ebert PR, Menzel R. 2001. Cloning of a catalytic subunit of cAMP-dependent protein kinase from the honeybee (Apis mellifera) and its localization in the brain. Insect Mol Biol 10:173-181.
Eisthen HL. 2002. Why are olfactory systems of different animals so similar? Brain Behav Evol 59:273-293.
Ertas B, von Reumont BM, Wägele JW, Misof B, Burmester T. 2009. Hemocyanin suggests a close relationship of Remipedia and Hexapoda. Mol Biol Evol 26:2711-2718.
Fahrbach SE. 2006. Structure of the mushroom bodies in the insect brain. Annu Rev Entomol 51:209-232.
Fanenbruck M, Harzsch S, Wägele JW. 2004. The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. Proc Natl Acad Sci USA 101:3868-3873.
Fanenbruck M, Harzsch S. 2005. A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships.
Arthropod Struct Dev 34:343-378.
Farris SM, Abrams AI, Strausfeld NJ. 2004. Development and morphology of Class II Kenyon cells in the mushroom bodies of the honey bee, Apis mellifera. J Comp Neurol 474:325-339.
Farris SM. 2005. Evolution of insect mushroom bodies: old clues, new insights. Arthropod Struct Dev 34:211-234.
Fiala A. 2007. Olfaction and olfactory learning in Drosophila: recent progress. Curr Opin Neurobiol 17:720-726.
Friedrich M, Tautz D. 1995. Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376:165-167.
Galizia CG, Rössler W. 2010. Parallel olfactory systems in insects: anatomy and function.
Annu Rev Entomol 55:399-420.
Galizia CG. 2014. Olfactory coding in the insect brain: data and conjectures. Eur J Neurosci
Haase A, Stern M, Wächtler K, Bicker G. 2001. A tissue-specific marker of Ecdysozoa. Dev Genes Evol 211:428-433.
Hallberg E, Johansson KUI, Elofsson R. 1992. The aesthetasc concept: structural variations of putative olfactory receptor cell complexes in crustacea. Microsc Res Tech 22:325-335.
Hammer M. 1997. The neural basis of associative reward learning in honeybees. Trends Neurosci 20:245-252.
Hanström B. 1928. Vergleichende Anatomie des Nervensystems der wirbellosen Tiere.
Springer, Berlin.
Harrison P, Macmillan D, Young H. 1995. Serotonin immunoreactivity in the ventral nerve cord of the primitive crustacean Anaspides tasmaniae closely resembles that of crayfish. J Exp Biol 198:531-535.
Harzsch S, Müller CH, Wolf H. 2005. From variable to constant cell numbers: cellular characteristics of the arthropod nervous system argue against a sister-group relationship of Chelicerata and "Myriapoda" but favour the Mandibulata concept. Dev Genes Evol 215:53-68.
Harzsch S, Rieger V, Krieger J, Seefluth F, Strausfeld NJ, Hansson BS. 2011. Transition from marine to terrestrial ecologies: changes in olfactory and tritocerebral neuropils in land-living isopods. Arthropod Struct Dev 40:244-257.
Harzsch S, Vilpoux K, Blackburn DC, Platchetzki D, Brown NL, Melzer R, Kempler KE, Battelle BA. 2006. Evolution of arthropod visual systems: development of the eyes and central visual pathways in the horseshoe crab Limulus polyphemus Linnaeus, 1758 (Chelicerata, Xiphosura). Dev Dyn 235:2641-2655.
Harzsch S, Waloszek D. 2000. Serotonin-immunoreactive neurons in the ventral nerve cord of Crustacea: a character to study aspects of arthropod phylogeny. Arthropod Struct Dev 29:307-322.
Harzsch S. 2003. Evolution of identified arthropod neurons: the serotonergic system in relation to engrailed-expressing cells in the embryonic ventral nerve cord of the american lobster Homarus americanus Milne Edwards, 1873 (Malacostraca, Pleocyemata, Homarida). Dev Biol 258:44-56.
Harzsch S. 2004. Phylogenetic comparison of serotonin-immunoreactive neurons in representatives of the Chilopoda, Diplopoda, and Chelicerata: implications for arthropod relationships. J Morphol 259:198-213.
Harzsch S. 2006. Neurophylogeny: Architecture of the nervous system and a fresh view on arthropod phylogeny. Integr Comp Biol 46:182-194.
Harzsch S. 2007. The architecture of the nervous system provides important characters for phylogenetic reconstructions: examples from the Arthropoda. Species Phylogeny Evol 1:33-57.
Hirsh J, Davidson N. 1981. Isolation and characterization of the dopa decarboxylase gene of Drosophila melanogaster. Mol Cell Biol 1:475-485.
Holmgren N. 1916. Zur Vergleichenden Anatomie des Gehirns von Polychaeten.
Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten.
Vorstudien zu einer Phylogenie der Arthropoden. Kungl Svenska Vetenskapsakad Handl 56:1-303.
Homberg U, Kingan TG, Hildebrand JG. 1987. Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248:1-24.
Homberg U. 1991. Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry.
J Comp Neurol 303:245-254.
Homberg U. 2002. Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189-209.
Homberg U. 2008. Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37:347-362.
Hörner M. 1999. Cytoarchitecture of histamine-, dopamine-, serotonin- and octopamine-containing neurons in the cricket ventral nerve cord. Microsc Res Tech 44:137-165.
Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W. 2001. Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154-157.
Ignell R, Anton S, Hansson BS. 2001. The antennal lobe of Orthoptera—anatomy and evolution. Brain Behav Evol 57:1-17.
Ignell R. 2001. Monoamines and neuropeptides in antennal lobe interneurons of the desert locust, Schistocerca gregaria: an immunocytochemical study. Cell Tissue Res 306:143-156.
Jenner RA. 2010. Higher-level crustacean phylogeny: consensus and conflicting hypotheses.
Arthropod Struct Dev 39:143-153.
Johansson KUI, Hallberg E. 1992. The organization of the olfactory lobes in Euphausiacea and Mysidacea (Crustacea, Malacostraca). Zoomorphology 112:81-90.
Karcavich R, Doe CQ. 2005. Drosophila neuroblast 7-3 cell lineage: a model system for studying programmed cell death, Notch/Numb signaling, and sequential specification of ganglion mother cell identity. J Comp Neurol 481:240-251.
Kenning M, Müller C, Wirkner CS, Harzsch S. 2013. The Malacostraca (Crustacea) from a neurophylogenetic perspective: new insights from brain architecture in Nebalia herbstii Leach, 1814 (Leptostraca, Phyllocarida). Zool Anz J Comp Zool 252:319-336.
Klemm N, Hustert R, Cantera R, Nässel DR. 1986. Neurons reactive to antibodies against serotonin in the stomatogastric nervous system and in the alimentary canal of locust and crickets (Orthoptera, Insecta). Neuroscience 17:247-261.
Koenemann S, Olesen J, Alwes F, Iliffe TM, Hoenemann M, Ungerer P, Wolff C, Scholtz G.
2009. The post-embryonic development of Remipedia (Crustacea) – additional results and new insights. Dev Genes Evol 219:131-145.
Koenemann S, Schram FR, Bloechl A, Hoenemann M, Iliffe TM, Held C. 2007. Post-embryonic development of remipede crustaceans. Evol Dev 9:117-121.
Kollmann M, Huetteroth W, Schachtner J. 2011. Brain organization in Collembola (springtails). Arthropod Struct Dev 40:304-316.
Kravitz EA. 1988. Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. Science 241:1775-1781.
Krieger J, Braun P, Rivera NT, Schubart CD, Müller CH, Harzsch S. 2015. Comparative analyses of olfactory systems in terrestrial crabs (Brachyura): evidence for aerial olfaction? PeerJ 3:e1433.
Krieger J, Sandeman RE, Sandeman DC, Hansson BS, Harzsch S. 2010. Brain architecture of the largest living land arthropod, the giant robber crab Birgus latro (Crustacea, Anomura, Coenobitidae): evidence for a prominent central olfactory pathway? Front Zool 7:25.
Kubrakiewicz J, Jaglarz MK, Iliffe TM, Bilinski SM, Koenemann S. 2012. Ovary structure and early oogenesis in the remipede, Godzilliognomus frondosus (Crustacea, Remipedia):
phylogenetic implications. Zoology 115:261-269.
Kutsch W, Breidbach O. 1994. Homologous structures in the nervous systems of Arthropoda.
Adv Insect Physiol 24:1-114.
Laurent G, Naraghi M. 1994. Odorant-induced oscillations in the mushroom bodies of the locust. J Neurosci 14:2993-3004.
Laurent G. 1996. Dynamical representations of odours by oscillating and evolving neural assemblies. Trends Neurosci 19:489-496.
Leitch B, Laurent G. 1996. GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J Comp Neurol 372:487-514.
Livingstone MS, Tempel BL. 1983. Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature 303:67-70.
Loesel R, Nässel DR, Strausfeld NJ. 2002. Common design in a unique midline neuropil in the brains of arthropods. Arthropod Struct Dev 31:77-91.
Loesel R, Richter S. 2014. Neurophylogeny - from description to character analysis. In:
Wägele JW, Bartholomäus T (eds). Deep Metazoan Phylogeny: The backbone of the Tree of Life. De Gruyter, Berlin, pp. 505-514.
Loesel R, Seyfarth EA, Bräunig P, Agricola HJ. 2011. Neuroarchitecture of the arcuate body in the brain of the spider Cupiennius salei (Araneae, Chelicerata) revealed by allatostatin-, proctolin-, and CCAP-immunocytochemistry and its evolutionary implications. Arthropod Struct Dev 40:210-220.
Loesel R, Wolf H, Kenning M, Harzsch S, Sombke A. 2013. Architectural principles and evolution of the arthropod central nervous system. In: Minelli A, Boxshall G, Fusco G (eds). Arthropod biology and evolution. Springer, Berlin, Heidelberg, pp. 299-342.
Loesel R. 2004. Comparative morphology of central neuropils in the brain of arthropods and its evolutionary and functional implications. Acta Biol Hung 55:39-51.
Longley AJ, Longley RD. 1986. Serotonin immunoreactivity in the nervous system of the dragonfly nymph. J Neurobiol 17:329-338.
Lundell MJ, Chu-LaGraff Q, Doe CQ, Hirsh J. 1996. The engrailed and huckebein genes are essential for development of serotonin neurons in the Drosophila CNS. Mol Cell Neurosci 7:46-61.
Mallatt JM, Garey JR, Shultz JW. 2004. Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol Phylogenet Evol 31:178-191.
McKinzie ME, Benton JL, Beltz BS, Mellon D. 2003. Parasol cells in the hemiellipsoid body of the crayfish Procambarus clarkii: dendritic branching patterns and functional implications. J Comp Neurol 462:168-179.
Mellon D Jr, Alones V, Lawrence MD. 1992. Anatomy and fine structure of neurons in the deutocerebral projection pathway of the crayfish olfactory system. J Comp Neurol 321:93-111.
Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG, Niehuis O, Petersen M, Izquierdo-Carrasco F, Wappler T, Rust J, Aberer AJ, Aspöck U, Aspöck H, Bartel D, Blanke A, Berger S, Böhm A, Buckley TR, Calcott B, Chen J, Friedrich F, Fukui M, Fujita M, Greve C, Grobe P, Gu S, Huang Y, Jermiin LS, Kawahara AY, Krogmann L, Kubiak M, Lanfear R, Letsch H, Li Y, Li Z, Li J, Lu H, Machida R, Mashimo Y, Kapli P, McKenna DD, Meng G, Nakagaki Y, Navarrete-Heredia JL, Ott M, Ou Y, Pass G, Podsiadlowski L, Pohl H, von Reumont BM, Schütte K, Sekiya K, Shimizu S, Slipinski A, Stamatakis A, Song W, Su X, Szucsich NU, Tan M, Tan X, Tang M, Tang J, Timelthaler G, Tomizuka S, Trautwein M, Tong X, Uchifune T, Walzl MG, Wiegmann BM, Wilbrandt J, Wipfler B, Wong TK, Wu Q, Wu G, Xie Y, olfactory pathway of Lepismachilis y-signata (Archaeognatha: Machilidae). Arthropod Struct Dev 40:317-333.
Moura G, Christoffersen ML. 1996. The system of the mandibulate arthropods: Tracheata and Remipedia as sister groups, ‘‘Crustacea’’ nonmonophyletic. J Comp Biol 1:95-113.
Nässel DR, Cantera R. 1985. Mapping of serotonin-immunoreactive neurons in the larval nervous system of the flies Calliphora erythrocephala and Sarcophaga bullata. Cell Tissue Res 239:423-434.
Nässel DR. 1988. Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurolbiol 30:1-85.
Neckameyer WS, White K. 1992. A single locus encodes both phenylalanine hydroxylase and tryptophan hydroxylase activities in Drosophila. J Biol Chem 267:4199-4206.
Neiber MT, Hartke TR, Stemme T, Bergmann A, Rust J, Iliffe TM, Koenemann S. 2011.
Global biodiversity and Phylogenetic Evaluation of Remipedia (Crustacea). PLoS One 6:e19627.
Novotny T, Eiselt R, Urban J. 2002. Hunchback is required for the specification of the early sublineage of neuroblast 7-3 in the Drosophila central nervous system. Development 129:1027-1036.
Oakley TH, Wolfe JM, Lindgren AR, Zaharoff AK. 2012. Phylotranscriptomics to bring the understudied into the fold: monophyletic Ostracoda, fossil placement and pancrustacean phylogeny. Mol Biol Evol 30:215-233.
Papadopoulou M, Cassenaer S, Nowotny T, Laurent G. 2011. Normalization for sparse encoding of odors by a wide-field interneuron. Science 332:721-725.
Paul DH. 1989. A neurophylogenist’s view of decapod Crustacea. Bull Mar Sci 45:487-504.
Paul DH. 1990. Neural phylogeny - its use in studying neural circuits. In: Wiese K, Krenz WD, Tautz J, Reichert H, Mulloney B. Frontiers in crustacean neurobiology. Birkhäuser Verlag, Basel, Boston, Berlin, pp. 537-546.
Peters BH, Butler SV, Tyrer NM. 1987. Morphology, ultrastructure and synapse distribution of putative serotonergic salivary neurons in the locust. Neuroscience 23:705-719.
Pfeiffer K, Homberg U. 2014. Organization and functional roles of the central complex in the insect brain. Annu Rev Entomol 59:165-184.
Pisani D, Poling LL, Lyons-Weiler M, Hedges SB. 2004. The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biol 2:1.
Polanska MA, Tuchina O, Agricola H, Hansson BS, Harzsch S. 2012. Neuropeptide
Polanska MA, Tuchina O, Agricola H, Hansson BS, Harzsch S. 2012. Neuropeptide