Worsaae Katrine, Rouan Alice, Seaver Elaine, Miyamoto Norio, Tilic Ekin
Marine Biological Section, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
The Whitney Laboratory for Marine Bioscience, University of Florida, Gainesville, FL, United States.
Front Neurosci. 2024 Mar 18;18:1369274. doi: 10.3389/fnins.2024.1369274. eCollection 2024.
Most species of the bone-devouring marine annelid, display distinct sexual dimorphism with macroscopic sedentary females rooted in bones and free-living microscopic dwarf males. The paedomorphic male resembles the non-feeding metatrochophore larva in size, presence of eight pairs of chaetae, and a head ciliation potentially representing a residual prototroch. The male development may thus uniquely reiterate and validate the theoretical heterochrony process "progenesis", which suggests that an accelerated sexual maturation and early arrest of somatic growth can lead to a miniaturized and paedomorphic adult. In this study, we describe the postembryonic larval and juvenile organogenesis of to test for a potential synchronous arrest of somatic growth during male development. Five postembryonic stages could be distinguished, resembling day one to five in the larval development at 10°C: (0D) first cleavage of fertilized eggs (embryos undergo unequal spiral cleavage), (1D) pre-trochophore, with apical organ, (2D) early trochophore, + prototroch, brain, circumesophageal connectives and subesophageal commissure, (3D) trochophore, + telotroch, four ventral nerves, (4D) early metatrochophore, + protonephridia, dorsal and terminal sensory organs, (5D) metatrochophore, + two ventral paratrochs, mid-ventral nerve, posterior trunk commissure, two dorsal nerves; competent for metamorphosis. The larval development largely mirrors that of other lecithotrophic annelid larvae but does not show continuous chaetogenesis or full gut development. Additionally, larvae exhibit an unpaired, mid-dorsal, sensory organ. Female individuals shed their larval traits during metamorphosis and continue organogenesis (including circulatory system) and extensive growth for 2-3 weeks before developing oocytes. In contrast, males develop sperm within a day of metamorphosis and display a synchronous metamorphic arrest in neural and muscular development, retaining a large portion of larval features post metamorphosis. Our findings hereby substantiate male miniaturization in to be the outcome of an early and synchronous offset of somatic development, fitting the theoretical process "progenesis". This may be the first compelling morpho-developmental exemplification of a progenetic origin of a microscopic body plan. The presented morphological staging system will further serve as a framework for future examination of molecular patterns and pathways determining development.
大多数噬骨海洋环节动物物种表现出明显的两性异形,雌性成虫体型较大,固定在骨骼中,而雄性则是自由生活的微小侏儒形态。幼态雄性在大小、具有八对刚毛以及头部纤毛(可能代表残留的原轮虫)方面类似于非摄食性的中轮幼虫。因此,雄性发育可能独特地重复并验证了理论上的异时过程“幼态发生”,该过程表明性成熟加速和体细胞生长早期停滞可导致成年个体小型化和幼态化。在本研究中,我们描述了[物种名称]胚胎后期幼虫和幼体的器官发生,以测试雄性发育过程中体细胞生长是否可能同步停滞。可以区分出五个胚胎后期阶段,类似于在10°C下幼虫发育的第1天至第5天:(0D)受精卵的第一次卵裂(胚胎进行不等螺旋卵裂),(1D)前担轮幼虫期,有顶器,(2D)早期担轮幼虫期,+原轮、脑、围食管连接和咽下神经连合,(3D)担轮幼虫期,+尾轮、四条腹神经,(4D)早期中轮幼虫期,+原肾管、背侧和末端感觉器官,(5D)中轮幼虫期,+两个腹侧副轮、腹侧中神经、后躯干连合、两条背神经;具备变态能力。幼虫发育在很大程度上反映了其他卵黄营养型环节动物幼虫的发育,但没有显示出连续的刚毛形成或完整的肠道发育。此外,[物种名称]幼虫表现出一个不成对的、中背侧感觉器官。雌性个体在变态过程中褪去幼虫特征,并在发育卵母细胞之前继续进行器官发生(包括循环系统)和广泛生长2 - 3周。相比之下,雄性在变态后一天内发育出精子,并在神经和肌肉发育方面表现出同步的变态停滞,变态后保留了大部分幼虫特征。我们的研究结果证实,[物种名称]中的雄性小型化是体细胞发育早期和同步偏移的结果,符合“幼态发生”的理论过程。这可能是微观体型计划幼态起源的第一个令人信服的形态发育例证。所呈现的形态分期系统将进一步作为未来研究决定[物种名称]发育的分子模式和途径的框架。