Kurtova A.I.1*, Girich A.S.2, Dolmatov I.Yu.2, Voronezhskaya E.E.1 2024. Divergence in developmental patterns of larval and adult nervous systems in direct-developing holothuria Eupentacta fraudatrix suggests their independent evolution // Invertebrate Zoology. Vol.21. No.2: 119–139 [in English].
1 Koltzov Institute of Developmental Biology Russian Academy of Sciences, Vavilova str. 26-1, Moscow 119334 Russia.
2 A.V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Palchevskogo str. 17, Vladivostok 690041 Russia.
* Corresponding author
Anastasia Kurtova: kurtova@idbras.ru ORCID 0000-0002-9713-7008
Alexander Girich: astromoon@mail.ru ORCID 0000-0003-2232-1182
Igor Dolmatov: idolmatov@mail.ru ORCID 0000-0003-3923-8131
Elena Voronezhskaya: elena.voronezhskaya@idbras.ru ORCID 0000-0002-9953-2538
doi: 10.15298/invertzool.21.2.01
ABSTRACT: The remarkable distinctions between the larval and adult nervous systems of echinoderms prompt inquiries into their potential developmental continuity and evolutionary origins. To address these questions, it is imperative to discern the conservative aspects of neurogenesis from its adaptive features related to the larval lifestyle. In this study, we explored the influence of direct development on the formation of both larval and adult nervous systems in Eupentacta fraudatrix, a species of holothurians with lecithotrophic larvae. Gastrula, vitellaria, and pentactula stages were analyzed via double labeling with antibodies targeting serotonin (5-HT) and acetylated α-tubulin (AcTub). First 5-HT-positive cells of the larval nervous system emerge in the ectoderm of the animal hemisphere during the gastrula stage. By the vitellaria stage, 5-HT-positive cells and fibers become concentrated in a band-like network surrounding the base of the preoral lobe. Notably, this network is exclusively superficial and lacks cell clusters resembling an apical organ. In the late vitellaria stage, AcTub-positive fibers become visible within this network. Upon settlement, 5-HT-positive elements disappear entirely, while some AcTub-positive fibers from the larval network persist in the basiepidermal regions of pentactula. Within the developing adult nervous system, AcTub staining reveals the formation of a circumoral nerve ring and a ventral cord at the vitellaria stage. Subsequently, five radial cords and a caudal nerve ring gradually emerge during settlement, leading to the establishment of a pentaradial nervous system in juveniles. No 5-HT-positive elements were detected among the rudiments of adult nervous system. Despite the coexistence of both larval and adult nervous systems for extended period during the vitellaria stage, no morphological connection between them was observed. Our findings revealed that the structure of the larval nervous system in E. fraudatrix exhibits significant differences from planktotrophic larvae of holothurians and shows a closer resemblance to the lecithotrophic larvae of other echinoderms. Meanwhile, the formation of the adult nervous elements in E. fraudatrix does not differ from that of holothurians with planktotrophic larvae. Thus, the lecithotrophic lifestyle appears to influence the structure of the larval nervous system, leaving the development of the adult nervous system unaffected. Consequently, these distinct nervous systems demonstrate disparate adaptive plasticity and likely evolved independently.
KEY WORDS: larval nervous system, vitellaria, pentactula, direct development, nerve cords, holothurians, echinoderms.