Molecular regionalization in the compact brain of the meiofaunal annelid Dinophilus gyrociliatus (Dinophilidae)

Abstract

BackgroundAnnelida is a morphologically diverse animal group that exhibits a remarkable variety in nervous system architecture (e.g., number and location of longitudinal cords, architecture of the brain). Despite this heterogeneity of neural arrangements, the molecular profiles related to central nervous system patterning seem to be conserved even between distantly related annelids. In particular, comparative molecular studies on brain and anterior neural region patterning genes have focused so far mainly on indirect-developing macrofaunal taxa. Therefore, analyses on microscopic, direct-developing annelids are important to attain a general picture of the evolutionary events underlying the vast diversity of annelid neuroanatomy.ResultsWe have analyzed the expression domains of 11 evolutionarily conserved genes involved in brain and anterior neural patterning in adult females of the direct-developing meiofaunal annelid Dinophilus gyrociliatus. The small, compact brain shows expression of dimmed, foxg, goosecoid, homeobrain, nk2.1, orthodenticle, orthopedia, pax6, six3/6 and synaptotagmin-1. Although most of the studied markers localize to specific brain areas, the genes six3/6 and synaptotagmin-1 are expressed in nearly all perikarya of the brain. All genes except for goosecoid, pax6 and nk2.2 overlap in the anterior brain region, while the respective expression domains are more separated in the posterior brain.ConclusionsOur findings reveal that the expression patterns of the genes foxg, orthodenticle, orthopedia and six3/6 correlate with those described in Platynereis dumerilii larvae, and homeobrain, nk2.1, orthodenticle and synaptotagmin-1 resemble the pattern of late larvae of Capitella teleta. Although data on other annelids are limited, molecular similarities between adult Dinophilus and larval Platynereis and Capitella suggest an overall conservation of molecular mechanisms patterning the anterior neural regions, independent from developmental and ecological strategies, or of the size and configuration of the nervous system.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-016-0058-2) contains supplementary material, which is available to authorized users.

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

“…Similar to previous findings in dinophilids (Müller & Westheide, ; Fofanova et al, ; Kerbl et al, ; b) and for example, C. teleta (which also shows a uniform, yet macroscopic brain (Fröbius & Seaver, ; Meyer & Seaver, ; Meyer et al, ), the seemingly homogeneous architecture of the brain does not negate the presence of clearly demarcated regions as indicated by expression patterns of different genes (Fröbius & Seaver, ; Meyer et al, ; Kerbl et al, ), as well as the immunoreactive patterns of some neuropeptides, which could be shown in this study to be localized in specific regions of the brain (e.g., Figures , , , and ).…”

“…The here employed set of specific neuropeptides complements previous studies using the common neural markers FMRFamide and serotonin (the former being represented in numerous somata, the latter being limited to three pairs of somata in the posterior dorsal region of the brain (this study, Müller & Westheide, ; Fofanova et al, ; Kerbl et al, )).…”

“…Detecting regionalization in these brains and in case of the herein presented D. gyrociliatus —putatively reflecting different functionality of specific brain areas—is not easily accomplished based on, for example, immunohistochemistry and CLSM (Müller & Westheide, ; Fofanova et al, ; Kerbl et al, ) or previous light microscopic studies (Nelson, ). However, a recent study on the molecular patterning of the compact D. gyrociliatus brain revealed demarcated expression areas of a set of 11 genes commonly related to (early) neural patterning, which do suggest a functional differentiation of the brain (Kerbl et al, ). Although the distribution of immunoreactive cells of this study could not be correlated with the exact expression patterns of these genes, both studies lead us to suggest that—rather than undifferentiated cell groups achieving multifunctionality in the microscopic brains of dinophilids—specific functionality is limited to few or individual cells.…”

“…taeniatus does not seem to be correlated with the formation of separated neuropil-compartments such as seen in the brains of macroscopic annelids such as Nereis viridens (Heuer & Loesel, 2007;Kulakova et al, 2007), Platynereis dumerilii (Fischer et al, 2010;Heuer et al, 2010) or Capitella teleta (Meyer & Seaver, 2009a). The Similar to previous findings in dinophilids (M€ uller & Westheide, 2002;Fofanova et al, 2014;Kerbl et al, 2016a; and for example, C. Seaver, 2006;Meyer & Seaver, 2009a,b;Meyer et al, 2015), the seemingly homogeneous architecture of the brain does not negate the presence of clearly demarcated regions as indicated by expression patterns of different genes (Fr€ obius & Seaver, 2006;Meyer et al, 2015;Kerbl et al, 2016b), as well as the immunoreactive patterns of some neuropeptides, which could be shown in this study to be localized in specific regions of the brain (e.g., Figures 5,9,12,16 and 20).…”

“…bodies recognizing annelid neuropeptides have been developed for the nereid annelid Platynereis dumerilii(Conzelmann et al, 2011;Conzelmann & J ekely, 2012;Shahidi et al, 2015;Williams et al, 2015;Williams et al, 2017). To check the conservation of the Platynereis peptides in the three species we searched in the available transcriptomes of D. gyrociliatus (SRX2030658,Kerbl et al, 2016b), D. taeniatus (SRX1025580,Andrade et al 2015) and T. axi (SRR2014693, Struck et al 2015), where we identified homologs for several Platynereis proneuropeptides in at least one of the species…”