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Evolution of Flatworm Central Nervous Systems: Insights from Polyclads

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Evolution of Flatworm Central Nervous Systems: Insights from Polyclads Genetics and Molecular Biology, 38, 3, 233-248 (2015) Copyright © 2015, Sociedade Brasileira de Genética. Printed in Brazil DOI: http://dx.doi.org/10.1590/S1415-475738320150013 Research Article Evolution of flatworm central nervous systems: Insights from polyclads Sigmer Y. Quiroga1,§, E. Carolina Bonilla3,§, D. Marcela Bolaños2,3,§, Fernando Carbayo4,5, Marian K. Litvaitis2 and Federico D. Brown3,5,6,7 1Programa de Biología, Facultad de Ciencias Básicas, Universidad del Magdalena, Santa Marta, Colombia. 2Department of Natural Resources and the Environment, University of New Hampshire, Durham, NH, USA. 3Laboratorio de Biología del Desarrollo, Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia. 4Laboratório de Ecologia e Evolução, Escola de Artes, Ciências e Humanidades, Universidade de São Paulo, São Paulo, SP, Brazil. 5Programa de Pós-Graduação em Zoologia, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil. 6Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil. 7Centro de Biologia Marinha, Universidade de São Paulo, São Sebastião, Brazil. Abstract The nervous systems of flatworms have diversified extensively as a consequence of the broad range of adaptations in the group. Here we examined the central nervous system (CNS) of 12 species of polyclad flatworms belonging to 11 different families by morphological and histological studies. These comparisons revealed that the overall organi- zation and architecture of polyclad central nervous systems can be classified into three categories (I, II, and III) based on the presence of globuli cell masses -ganglion cells of granular appearance-, the cross-sectional shape of the main nerve cords, and the tissue type surrounding the nerve cords. In addition, four different cell types were iden- tified in polyclad brains based on location and size. We also characterize the serotonergic and FMRFamidergic ner- vous systems in the cotylean Boninia divae by immunocytochemistry. Although both neurotransmitters were broadly expressed, expression of serotonin was particularly strong in the sucker, whereas FMRFamide was particularly strong in the pharynx. Finally, we test some of the major hypothesized trends during the evolution of the CNS in the phylum by a character state reconstruction based on current understanding of the nervous system across different species of Platyhelminthes and on up-to-date molecular phylogenies. Keywords: brain, FMRFamide, globuli cell masses, orthogon, serotonin. Received: January 13, 2015; Accepted: April 19, 2015. Introduction (Laumer et al., 2015; Egger et al., 2015). The main charac- Current phylogenetic views of Platyhelminthes di- teristic of the Polycladida is their highly branched intestine vide the phylum into Catenulida and Rhabditophora (Lau- (Hyman, 1951), from which they derive their name. Poly- mer and Giribet, 2014; Laumer et al,. 2015; Egger et al., clads have few external traits; however, the presence or ab- 2015). Within the diverse Rhabditophora, strong morpho- sence of clusters of eyespots and either true tentacles or logical and molecular evidence suggests Macrostomorpha pseudotentacles, which form by folds of the anterior body as the basal clade; whereas Polycladida, often considered a margin, can be used as systematic characters (Newman and basal clade (for a review see Baguñà and Riutort, 2004; Cannon, 1994). The initial division of the order is based on Karling, 1967, 1974; Carranza et al,. 1997, Litvaitis and the presence or absence of a ventral sucker. This character Rhode, 1999; Laumer and Giribet, 2014), currently groups divides the polyclads into the two suborders Acotylea together with the Prorhynchida in a more derived position (without sucker) and Cotylea (with sucker) (Lang, 1884). based on recent phylogenomic and transcriptomic analyses Among invertebrates, nervous systems exhibit a wide variety of organization, which can range from an unorga- Send correspondence to Federico D. Brown. Departamento de nized diffuse nerve net (cnidarians) to complex systems Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, No. 101, Cidade Universitária, 05508-090 with highly specialized sensory receptors (arthropods, São Paulo, SP, Brazil. E-mail: [email protected]. some mollusks) (Ruppert and Barnes, 1994). The bilater- §These authors contributed equally to the present work. ally flattened body of flatworms preserves a common orga- 234 Quiroga et al. nization of the central nervous system (CNS). The CNS of As part of a comprehensive and comparative study of flatworms consists of: (i) the orthogon, composed of main ca. 20 species of polyclads from the Gulf of Naples, Lang longitudinal nerve cords and transverse commissures that (1884) unified early descriptions of the main morphologi- form a ladder-like network. The main cords have direct cal features in polyclad nervous systems. Detailed histo- connections to the brain, are generally multifibrillar, are logical descriptions of the CNS are available for the coty- more strongly developed on the ventral side, and express lean, Thysanozoon brocchii Risso, 1818 (Lang, 1884) and serotonin or cholinergic neuropeptides (Reuter and Gus- more recently for the acotylean, Notoplana acticola Boone, tafsson, 1995). The number, position, and arrangement of 1929 (Koopowitz, 1973, 1986; Chien and Koopowitz, cords vary drastically from one taxonomic group to the 1972, 1977; Koopowitz and Chien, 1974, 1975). The CNS next; (ii) an anterior brain consisting of two lobes con- consists of an anterior, bilobed brain that functions in coor- nected by one or several commissures. The lobes may be ei- dinating locomotion and peripheral reflex activity (Koopo- ther loosely aggregated or encapsulated by a sheath of witz, 1973). In both species, this brain is enclosed by a dis- extracellular matrix (Reuter and Gustafsson, 1995); and tinct capsule and is composed of an outer rind of cells, (iii) the plexus, composed of a network of sub- and infra- formed by a variety of neuronal types (e.g., multipolar, de- epidermal, or submuscular nerves that expand throughout cussating, coupled), and an inner core of thin fibers and a the body of the worm. In addition, in free-living flatworms complete lack of nuclei or cell bodies (Lang, 1884; Koopo- the presence of pharyngeal and stomatogastric plexi, con- witz, 1986). In T. brocchii, the largest, multipolar ganglion sisting of either one or two nerve rings, innervated by sub- cells are mostly confined to the dorsal, ventral, and poste- and infra-epithelial nerve nets (Reuter and Gustafsson, rior parts of the brain. Thin fibers in the core of the brain 1995; Halton and Gustafsson, 1996), are considered plesio- form a complex anastomosing network, which gives rise to morphic characters (Ehlers, 1985). the nerve cords exiting the brain (Lang, 1884). At the front Reisinger (1925) defined a standard orthogonal pat- of each brain lobe and located outside the capsule are two tern for many free-living forms. This pattern consists of groups of sensory ganglion cells (globuli cell masses, or several pairs of ventral, lateral, and dorsal longitudinal Körnerhaufen in the original German terminology) that are nerve cords that are connected at right angles along their of granular appearance. Furthermore, Stylochoplana lengths by transverse commissures, forming a ladder-like maculata Quatrefage, 1845, N. acticola, Planocera Lang, arrangement. Although the orthogon organization and oc- 1879, and Gnesioceros Diesing, 1862 showed six pairs of currence does not show clear evolutionary trends (Reuter nerve cords radiating from the brain and forming a typical and Gustafsson, 1995), a common origin of the CNS in radial network pattern for the group (Koopowitz, 1973). flatworms has been suggested with convergent evolution of The first two pairs are directed forward (anterior and ante- similar orthogonal organizations in different taxa (Koti- rior dorsal nerves), the third and fourth pairs (lateral and lat- kova, 1991). The orthogon varies in position and number of eral dorsal nerves) are directed laterally from the brain, and cords, different points of contact with the brain, and thick- the last two pairs (posterior and posterior dorsal nerves) are ness of cords. Reuter et al. (1998) determined that the main directed posteriorly. These nerves soon branch repeatedly cords derive from strong roots in the brain, are composed of towards the margin, becoming more delicate and forming numerous neurons within wide fiber bundles, and generally anastomosing plexi that contain multi- and bipolar neurons show immunoreactivity for serotonin and catecholamines. (Koopowitz, 1974, 1986). It has been hypothesized that more derived clades often Neuroactive molecules can be classified broadly into have fewer but thicker nerve cords than more basal taxa neurotransmitters (e.g., acetylcholine, serotonin (5-HT), (Reisinger, 1972; Reuter and Gustafsson, 1995), and that GABA, histamine), neuropeptides (e.g., FMRF-amide) and longitudinal cords may have evolved from the fusion of nitric oxide, a dissolved gas with nervous and endocrine plexal fibers of ancestral taxa (Joffe and Reuter, 1993). function. In flatworms, immunocytochemistry (ICC) has The architecture of the polyclad nervous system re- demonstrated the presence of several neuroactive mole- flects components of the anatomically diffuse cnidarian cules, including typical neurotransmitters, nitric oxide syn- system
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