High diversity in neuropeptide immunoreactivity patterns among three closely related species of Dinophilidae (Annelida)

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Studies on the annelid brain and major nerves conducted by serial sectioning and TEM‐studies go back several decades (Windoffer & Westheide, 1988a; Purschke, 1993; Orrhage & Müller, 2005). The advancements in immunocytochemistry in combination with CLSM facilitated new neural descriptions in a broad range of invertebrates and has proven especially well‐suited for studies on microscopic representatives (e.g., meiofaunal taxa or temporary meiofauna such as embryos, larvae and juveniles of macroscopic species), where not only the nervous system but also its intricate relation to musculature and ciliated structures can be exposed (e.g., Hay‐Schmidt, 1992; Müller & Sterrer, 2004; Wanninger, Koop, Bromham, Noonan, & Degnan, 2005; McDougall, Chen, Shimeld, & Ferrier, 2006; Worsaae & Rouse, 2008; Nielsen & Worsaae, 2010; Worsaae & Rouse, 2010; Schwaha & Wanninger, 2012; Worsaae, Sterrer, Kaul‐Strehlow, Hay‐Schmidt, & Giribet, 2012; Kerbl, Bekkouche, Sterrer, & Worsaae, 2015; Schmidt‐Rhaesa, Harzsch, & Purschke, 2015; Bekkouche & Worsaae, 2016a; 2016b; Rimskaya‐Korsakova, Kristof, Malakhov, & Wanninger, 2016; Worsaae, Rimskaya‐Korsakova, & Rouse, 2016; Kerbl, Fofanova, Mayorova, Voronezhskaya, & Worsaae, 2016a; Gasiorowski, Bekkouche, & Worsaae, 2017; Henne, Friedrich, Hammel, Sombke, & Schmidt‐Rhaesa, 2017a; Henne, Sombke, & Schmidt‐Rhaesa, 2007b). Yet, few studies have taken advantage of the small‐sized meiofauna for studying the distribution of the numerous and proposedly highly conserved neuropeptides in adult nervous systems, using immunocytochemistry to identify putative morphological or functional regionalizations in their small and compact brain and nervous system.
Recent studies on invertebrates have shown that proneuropeptides (larger biologically inactive precursor proteins, which get cleaved and converted into neuropeptides) are conserved and orthologous peptides with only slight alternations, can be identified across most protostomes (Jékely, 2013). Furthermore, the immunoreactivity patterns of several neuropeptides could be shown to be rather similar among spiralian larvae of, annelids and molluscs, for example (Conzelmann & Jékely, 2012), suggesting that patterns of a more comprehensive range of neuropeptides may inform on deep homologies and ancestral functionalities in the nervous system (Conzelmann & Jékely, 2012). However, we lack detailed comparative analyses of a broader range of neuropeptide markers in closely related species to inform on homology versus homoplasticity of specific expression patterns (Verleyen et al., 2004; Henne et al., 2017a). Complementary analyses of adult microscopic brains would be relevant due to their comparably low cell number, which makes the examination of the adult brain anatomy and neurotransmitter immunoreactivity among closely related species more comprehensible. Furthermore, the relevance of microscopic animals for spiralian phylogenies was recently emphasized, with these branching off as early lineages within Spiralia, Ecdysozoa, and Bilateria (Andrade et al., 2015; Laumer et al., 2015; Struck et al., 2015; Cannon et al., 2016).
Many brains of macroscopic invertebrates (prime examples being cephalopods and insects, but also annelids such as Nereis) show structural compartmentalization in the form of lobes or ganglia (Young, 1971; Uyeno & Kier, 2005; Heuer & Loesel, 2007; Wollesen, Loesel, & Wanninger, 2009; Cardona et al., 2010; Lam et al., 2010; Heuer, Müller, Todt, & Loesel, 2010; Aso et al., 2014). These subregions of the brain include cells with common function to either directly process sensory input or serve as higher organization/integration centers (Uyeno & Kier, 2005; Williamson & Chrachri, 2007). Many small annelids, however, have seemingly uniform brains without any obvious ganglionic substructure (Müller & Westheide, 2002; Worsaae & Rouse, 2008; Meyer & Seaver, 2009a; Kerbl et al., 2016a). This raises the question of whether (and how) these brains are regionalized and whether neurons are multifunctional and thereby less specific for individual neurotransmitters.
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