Early embryogenesis and organogenesis in the annelid Owenia fusiformis

Abstract

Background Annelids are a diverse group of segmented worms within Spiralia, whose embryos exhibit spiral cleavage and a variety of larval forms. While most modern embryological studies focus on species with unequal spiral cleavage nested in Pleistoannelida (Sedentaria + Errantia), a few recent studies looked into Owenia fusiformis, a member of the sister group to all remaining annelids and thus a key lineage to understand annelid and spiralian evolution and development. However, the timing of early cleavage and detailed morphogenetic events leading to the formation of the idiosyncratic mitraria larva of O. fusiformis remain largely unexplored. Results Owenia fusiformis undergoes equal spiral cleavage where the first quartet of animal micromeres are slightly larger than the vegetal macromeres. Cleavage results in a coeloblastula approximately 5 h post-fertilization (hpf) at 19 °C. Gastrulation occurs via invagination and completes 4 h later, with putative mesodermal precursors and the chaetoblasts appearing 10 hpf at the dorso-posterior side. Soon after, at 11 hpf, the apical tuft emerges, followed by the first neurons (as revealed by the expression of elav1 and synaptotagmin-1) in the apical organ and the prototroch by 13 hpf. Muscles connecting the chaetal sac to various larval tissues develop around 18 hpf and by the time the mitraria is fully formed at 22 hpf, there are FMRFamide+ neurons in the apical organ and prototroch, the latter forming a prototrochal ring. As the mitraria feeds, it grows in size and the prototroch expands through active proliferation. The larva becomes competent after ~ 3 weeks post-fertilization at 15 °C, when a conspicuous juvenile rudiment has formed ventrally. Conclusions Owenia fusiformis embryogenesis is similar to that of other equal spiral cleaving annelids, supporting that equal cleavage is associated with the formation of a coeloblastula, gastrulation via invagination, and a feeding trochophore-like larva in Annelida. The nervous system of the mitraria larva forms earlier and is more elaborated than previously recognized and develops from anterior to posterior, which is likely an ancestral condition to Annelida. Altogether, our study identifies the major developmental events during O. fusiformis ontogeny, defining a conceptual framework for future investigations.

Dinophiliformia early neurogenesis suggests the evolution of conservative neural structures across the Annelida phylogenetic tree

“…Antibodies against acetylated tubulin, the neuropeptide RFamide, and the monoamine transmitter serotonin label individual neurons and their processes, as well as tubulin-containing ciliary structures ( Schmidt-Rhaesa, Harzsch & Purschke, 2015 ). The specificity of the antibodies used in our study has previously been shown in various representatives of lophotrochozoan taxa including mollusks and annelids ( Voronezhskaya & Elekes, 1996 ; Dickinson, Croll & Voronezhskaya, 2000 ; Voronezhskaya, Tsitrin & Nezlin, 2003 ; Wanninger et al, 2005 ; Kristof, Wollesen & Wanninger, 2008 ; Dyachuk & Odintsova, 2009 ; Fischer, Henrich & Arendt, 2010 ; Carrillo-Baltodano et al, 2019 ; Kumar et al, 2020 ; Carrillo-Baltodano et al, 2021 ).…”

“… The diagram is based on the recent data on Sedentaria ( Kumar et al, 2020 ); Errantia ( Starunov, Voronezhskaya & Nezlin, 2017 ); Dinophiliformia ( this study ); Sipuncula ( Carrillo-Baltodano et al, 2019 ), and Oweniidae ( Carrillo-Baltodano et al, 2021 ). The phylogeny data is retrieved from ( Martín-Durán et al, 2021 ).…”

Detailed morphology of tentacular apparatus and central nervous system in Owenia borealis (Annelida, Oweniidae)

“…: sections 69–78: morphdbase.de/?P_Beckers_20170310-M-96.1). According to some data [ 12 , 16 ], in the post-metamorphic stage of O. fusiformis, the dorsal root of the circumesophageal connectives contains 5HT-lir and FMRFamide-lir neurites, whereas the ventral root has only 5HT-lir neurites. In the adult oweniids, both the 5HT-lir and FMRFamide-lir nerves are also found in the rings of the anterior nerve center of G. oculata [ 13 ] and O. fusiformis [ 15 ].…”

“…[ 2 – 7 ]. Members of the family Oweniidae have many unusual morphological, ultrastructural, and developmental characteristics [ 8 – 16 ]. Oweniids together with magelonids have been recently placed among the Palaeoannelida, a sister group to all remaining annelids [ 5 , 7 ].…”

Dinophiliformia early neurogenesis suggests the evolution of conservative neural structures across the Annelida phylogenetic tree

“…Antibodies against acetylated tubulin, the neuropeptide RFamide, and the monoamine transmitter serotonin label individual neurons and their processes, as well as tubulin-containing ciliary structures (Schmidt-Rhaesa, Harzsch & Purschke, 2015). The specificity of the antibodies used in our study has previously been shown in various representatives of lophotrochozoan taxa including mollusks and annelids (Voronezhskaya & Elekes, 1996;Dickinson, Croll & Voronezhskaya, 2000;Voronezhskaya, Tsitrin & Nezlin, 2003;Wanninger et al, 2005;Kristof, Wollesen & Wanninger, 2008;Dyachuk & Odintsova, 2009;Fischer, Henrich & Arendt, 2010;Carrillo-Baltodano et al, 2019;Kumar et al, 2020;Carrillo-Baltodano et al, 2021).…”