Editorial Preface for Special Issue “Reproduction in Sponges: Diversity, Strategies, and Regulation”

IF 2.6 3区 生物学 Q3 BIOCHEMISTRY & MOLECULAR BIOLOGY
Alexander V. Ereskovsky, Andrey I. Lavrov
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Despite numerous debates regarding who diverged first, Porifera or Ctenophora, sponges remain a key group for understanding such fundamental questions as the origin of animal multicellularity and mechanisms of tissue integration, evolution of epithelium and nervous system, etc. From the Evo-Devo point of view, studies of sponges are crucial to shed light upon the nature of the somatic/germ line segregation in animals, the origin and early evolution of gametogenesis, embryonic and postembryonic development, asexual reproduction, regeneration, and morphogenesis itself (Lanna <span>2015</span>; Colgren and Nichols <span>2019</span>).</p><p>Despite more than 170 years of sponge developmental research (Ereskovsky <span>2010</span>; Cajado and Lanna, this issue), many obscure and unexplored topics remain in the developmental biology of these ancient animals. While sharing the basic features of reproduction (gametogenesis, fertilization, development from zygote, active cell movements during embryonic development, etc.) with eumetazoans, sponges demonstrate a great diversity of reproduction strategies and regulation, morphogenesis, and cell behavior, many of which are unique for the phylum. This special issue, “Reproduction in Sponges: Diversity, Strategies, and Regulation,” aims to present some of these poorly explored aspects in the developmental biology of Porifera.</p><p>Sponges demonstrate remarkably diverse sexual systems, ranging from stable gonochorism to sequential hermaphroditism and sex reversal (Sarà. <span>1993</span>). Surprisingly, the sexual system can be labile even with a single species being changed from year to year (Fell and Jacob <span>1979</span>). Furthermore, mechanisms of sex determination in sponges are poorly documented because studies are at least partially hindered by the absence of sexual dimorphism and structurally separated gonads in these animals. Lorente-Sorolla and Riesgo contribute a review that synthesizes the current knowledge on the sexual systems, environmental and genetic cues driving sexual fate, and the evolutionary origins of sexual conditions in sponges. They scrupulously analyze the scarce evidence of environmental and genotypic sex determination in sponges, giving proper attention to physiological and organizational features of these animals. Overall, Lorente-Sorolla and Riesgo argue that sponges exhibit an evolutionarily labile system in which sexual fate may emerge from the interaction of conserved genetic modules, environmental cues, and physiological constraints.</p><p>In turn, Cajado and Lanna present a wide and unique historical panorama of studies of reproduction and development in calcareous sponges for the last 200 years. Scrutinizing over 200 articles ranging from 1825 to 2026, the authors not only present a vast historical perspective on our visions of calcareous sponge developmental biology, but they also provide the current state of knowledge in this area, identify critical unanswered questions, and outline priorities for future research, making this review an exceptional framework for any researcher diving into the developmental biology of sponges.</p><p>The studies of the molecular mechanisms guiding the animal body plan formation through embryonic development are a cutting-edge research area in Evo-Devo for the last few decades (Gilbert and Barresi <span>2016</span>). However, studies focusing on non-bilaterian species are still few (Lanna <span>2015</span>; Degnan et al. <span>2015</span>). Borisenko et al. present the bulk transcriptomic analysis of embryogenesis in demosponge <i>Halisarca dujardinii</i> supplemented with the visualization of the spatial pattern of gene expression using whole-mount in situ hybridization. Authors characterize gene expression across three key stages: cleavage, blastula, and prelarva. They identified significant transcriptional shifts and analyzed the expression of numerous transcriptional factors as promising proxies controlling gene regulatory networks and major morphological rearrangements. Overall, the study by Borisenko et al. gives new insights into how morphologically simple animals utilize complex molecular mechanisms for their development.</p><p>Despite the long research history, the embryonic development in many sponge orders remains completely unknown. Nonetheless, the collected data provide a rich material for comparative embryological studies: it shows that the embryonic development in sponges is surprisingly diverse, and eight main developmental types are identified across various phylogenetic lines and different taxa (Ereskovsky <span>2004</span>, <span>2010</span>). Among the developmental types, the direct development (without larvae) in viviparous demosponges has been the least studied so far. Cárdenas et al. present a detailed description of the direct embryonic development in four <i>Craniella</i> species (Tetractinellida) with extensive histological studies. Previously, the direct embryonic development was studied histologically only once in another demosponge, <i>Stylocordyla chupachups</i> (Sarà et al. <span>2002</span>). The results obtained by Cárdenas et al. corroborate the distinction of the direct, non-larval development as a separate type of sponge embryonic development.</p><p>Metamorphosis is one of the key stages in sponge development. It entails a fundamental restructuring from the larval to the adult body plan. This developmental period is marked by the reestablishment of the main body axis and profound transdifferentiation of larval cells. The sponge metamorphosis has attracted considerable attention from researchers since the 19th century. And many of these studies are dealing with the metamorphosis of calcareous sponges (Ereskovsky <span>2010</span>; Cajado and Lanna, this issue) as they are the only sponge class giving opportunity to explore the emergence of various types of the aquiferous system. Lanna and Klautau characterized the morphogenetic processes during metamorphosis and aquiferous system development in two calcareous sponges: syconoid <i>Sycettusa hastifera</i> and, for the first time, in leuconoid <i>Paraleucilla magna</i>. In both species, the development of the adult aquiferous system starts with the asconoid system of the young olynthus and proceeds through the epithelial morphogenesis, but of different types. The description of the post-embryonic development of <i>S. hastifera</i> and <i>P. magna</i> will allow these species to be used as models in future experimental studies investigating morphogenesis during embryonic development and post-embryogenesis in sponges that were fundamental not only to the evolution of Porifera but also to the entire Metazoa.</p><p>Finally, the review by Ereskovsky and Lavrov provides a current critical overview of the modes of asexual reproduction in sponges. 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引用次数: 0

Abstract

Sponges have long fascinated biologists, and they remain central to Evo-Devo research. This status rests on their phylogenetic position as one of the early-diverging metazoan groups and on their unique anatomical and histological organization. Despite numerous debates regarding who diverged first, Porifera or Ctenophora, sponges remain a key group for understanding such fundamental questions as the origin of animal multicellularity and mechanisms of tissue integration, evolution of epithelium and nervous system, etc. From the Evo-Devo point of view, studies of sponges are crucial to shed light upon the nature of the somatic/germ line segregation in animals, the origin and early evolution of gametogenesis, embryonic and postembryonic development, asexual reproduction, regeneration, and morphogenesis itself (Lanna 2015; Colgren and Nichols 2019).

Despite more than 170 years of sponge developmental research (Ereskovsky 2010; Cajado and Lanna, this issue), many obscure and unexplored topics remain in the developmental biology of these ancient animals. While sharing the basic features of reproduction (gametogenesis, fertilization, development from zygote, active cell movements during embryonic development, etc.) with eumetazoans, sponges demonstrate a great diversity of reproduction strategies and regulation, morphogenesis, and cell behavior, many of which are unique for the phylum. This special issue, “Reproduction in Sponges: Diversity, Strategies, and Regulation,” aims to present some of these poorly explored aspects in the developmental biology of Porifera.

Sponges demonstrate remarkably diverse sexual systems, ranging from stable gonochorism to sequential hermaphroditism and sex reversal (Sarà. 1993). Surprisingly, the sexual system can be labile even with a single species being changed from year to year (Fell and Jacob 1979). Furthermore, mechanisms of sex determination in sponges are poorly documented because studies are at least partially hindered by the absence of sexual dimorphism and structurally separated gonads in these animals. Lorente-Sorolla and Riesgo contribute a review that synthesizes the current knowledge on the sexual systems, environmental and genetic cues driving sexual fate, and the evolutionary origins of sexual conditions in sponges. They scrupulously analyze the scarce evidence of environmental and genotypic sex determination in sponges, giving proper attention to physiological and organizational features of these animals. Overall, Lorente-Sorolla and Riesgo argue that sponges exhibit an evolutionarily labile system in which sexual fate may emerge from the interaction of conserved genetic modules, environmental cues, and physiological constraints.

In turn, Cajado and Lanna present a wide and unique historical panorama of studies of reproduction and development in calcareous sponges for the last 200 years. Scrutinizing over 200 articles ranging from 1825 to 2026, the authors not only present a vast historical perspective on our visions of calcareous sponge developmental biology, but they also provide the current state of knowledge in this area, identify critical unanswered questions, and outline priorities for future research, making this review an exceptional framework for any researcher diving into the developmental biology of sponges.

The studies of the molecular mechanisms guiding the animal body plan formation through embryonic development are a cutting-edge research area in Evo-Devo for the last few decades (Gilbert and Barresi 2016). However, studies focusing on non-bilaterian species are still few (Lanna 2015; Degnan et al. 2015). Borisenko et al. present the bulk transcriptomic analysis of embryogenesis in demosponge Halisarca dujardinii supplemented with the visualization of the spatial pattern of gene expression using whole-mount in situ hybridization. Authors characterize gene expression across three key stages: cleavage, blastula, and prelarva. They identified significant transcriptional shifts and analyzed the expression of numerous transcriptional factors as promising proxies controlling gene regulatory networks and major morphological rearrangements. Overall, the study by Borisenko et al. gives new insights into how morphologically simple animals utilize complex molecular mechanisms for their development.

Despite the long research history, the embryonic development in many sponge orders remains completely unknown. Nonetheless, the collected data provide a rich material for comparative embryological studies: it shows that the embryonic development in sponges is surprisingly diverse, and eight main developmental types are identified across various phylogenetic lines and different taxa (Ereskovsky 2004, 2010). Among the developmental types, the direct development (without larvae) in viviparous demosponges has been the least studied so far. Cárdenas et al. present a detailed description of the direct embryonic development in four Craniella species (Tetractinellida) with extensive histological studies. Previously, the direct embryonic development was studied histologically only once in another demosponge, Stylocordyla chupachups (Sarà et al. 2002). The results obtained by Cárdenas et al. corroborate the distinction of the direct, non-larval development as a separate type of sponge embryonic development.

Metamorphosis is one of the key stages in sponge development. It entails a fundamental restructuring from the larval to the adult body plan. This developmental period is marked by the reestablishment of the main body axis and profound transdifferentiation of larval cells. The sponge metamorphosis has attracted considerable attention from researchers since the 19th century. And many of these studies are dealing with the metamorphosis of calcareous sponges (Ereskovsky 2010; Cajado and Lanna, this issue) as they are the only sponge class giving opportunity to explore the emergence of various types of the aquiferous system. Lanna and Klautau characterized the morphogenetic processes during metamorphosis and aquiferous system development in two calcareous sponges: syconoid Sycettusa hastifera and, for the first time, in leuconoid Paraleucilla magna. In both species, the development of the adult aquiferous system starts with the asconoid system of the young olynthus and proceeds through the epithelial morphogenesis, but of different types. The description of the post-embryonic development of S. hastifera and P. magna will allow these species to be used as models in future experimental studies investigating morphogenesis during embryonic development and post-embryogenesis in sponges that were fundamental not only to the evolution of Porifera but also to the entire Metazoa.

Finally, the review by Ereskovsky and Lavrov provides a current critical overview of the modes of asexual reproduction in sponges. While asexual reproduction is widespread in sponges and has even become an integral part of an animal's life cycle in many sponge species, it remained on the margins of sponge development investigation for a long time. However, in recent decades, some forms of asexual reproduction (gemmulation in freshwater demosponges and budding in marine homoscleromorphs) have emerged as promising models for Evo-Devo studies (Funayama 2010; Okamoto et al. 2012; Rocher et al. 2024; Leys et al. 2025). In their review, Ereskovsky and Lavrov have summarized available data on the morphogenesis accompanying different types of asexual reproduction in four sponge classes and indicate aspects of sponge asexual reproduction requiring research in the future.

With this issue, we hope to shed light on several current questions in sponge developmental and reproductive biology. We believe this collection of research and review articles will not only interest developmental and evolutionary biologists but also inspire new research on this fascinating group of animals.

Alexander V. Ereskovsky: conceptualization, writing – original draft. Andrey I. Lavrov: conceptualization, writing – original draft.

Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

特刊“海绵的繁殖:多样性,策略和调节”社论序言。
长期以来,海绵一直吸引着生物学家,它们仍然是Evo-Devo研究的核心。这种状态取决于它们作为早期分化的后生动物群之一的系统发育地位以及它们独特的解剖和组织学组织。尽管关于海绵目和栉水母目谁先分化有很多争论,但海绵仍然是理解动物多细胞起源和组织整合机制、上皮和神经系统进化等基本问题的关键群体。从Evo-Devo的角度来看,对海绵的研究对于阐明动物体内体细胞/生殖系分离的本质、配子体发生的起源和早期进化、胚胎和胚胎后发育、无性生殖、再生和形态发生本身至关重要(Lanna 2015; Colgren and Nichols 2019)。尽管已有170多年的海绵发育研究(Ereskovsky 2010; Cajado and Lanna,本期),这些古老动物的发育生物学中仍然存在许多模糊和未探索的主题。虽然海绵动物与真生动物具有相同的基本生殖特征(配子体发生、受精、受精卵发育、胚胎发育过程中的活跃细胞运动等),但海绵动物在生殖策略和调控、形态发生和细胞行为方面表现出极大的多样性,其中许多特征是该门动物所独有的。本期特刊“海绵的繁殖:多样性、策略和调控”旨在介绍Porifera发育生物学中一些尚未被充分探索的方面。海绵表现出显著的多样化的性系统,从稳定的雌雄同体到顺序的雌雄同体和性别反转(sarcom)。1993)。令人惊讶的是,即使一个物种每年都在变化,性系统也可能是不稳定的(Fell and Jacob 1979)。此外,海绵性别决定的机制文献很少,因为这些动物缺乏两性二态性和结构上分离的性腺,至少部分阻碍了研究。Lorente-Sorolla和Riesgo撰写了一篇综述,综合了目前关于性系统、驱动性命运的环境和遗传线索以及海绵性条件的进化起源的知识。他们仔细分析了海绵中环境和基因型性别决定的稀缺证据,对这些动物的生理和组织特征给予了适当的关注。总的来说,Lorente-Sorolla和Riesgo认为海绵表现出一种进化上不稳定的系统,在这种系统中,性别命运可能来自保守的遗传模块、环境线索和生理限制的相互作用。反过来,Cajado和Lanna展示了过去200年来钙质海绵繁殖和发育研究的广泛而独特的历史全景。回顾了从1825年到2026年的200多篇文章,作者不仅展示了我们对钙质海绵发育生物学的看法的广阔历史视角,而且还提供了这一领域的知识现状,确定了关键的未解决的问题,并概述了未来研究的优先事项,使本综述成为任何研究海绵发育生物学的研究人员的特殊框架。通过胚胎发育引导动物体表形成的分子机制研究是近几十年来Evo-Devo的前沿研究领域(Gilbert and Barresi 2016)。然而,关注非双边物种的研究仍然很少(Lanna 2015; Degnan et al. 2015)。Borisenko等人对海参海绵(haisarca dujardinii)胚胎发生进行了大量转录组学分析,并利用全载原位杂交技术对基因表达的空间模式进行了可视化。作者描述了三个关键阶段的基因表达:卵裂、囊胚和前幼虫。他们发现了重要的转录变化,并分析了许多转录因子的表达,这些转录因子是控制基因调控网络和主要形态重排的有希望的代理。总的来说,Borisenko等人的研究为形态学简单的动物如何利用复杂的分子机制进行发育提供了新的见解。尽管研究历史悠久,但许多海绵目的胚胎发育仍是完全未知的。尽管如此,收集到的数据为比较胚胎学研究提供了丰富的材料:它表明海绵的胚胎发育具有惊人的多样性,在不同的系统发育系和不同的分类群中确定了八种主要的发育类型(Ereskovsky 2004, 2010)。在所有发育类型中,胎生蠕形海绵的直接发育(不含幼虫)是迄今为止研究最少的。Cárdenas等。 本文详细描述了四种颅属动物(四铁门)的直接胚胎发育,并进行了广泛的组织学研究。在此之前,直接胚胎发育的组织学研究只在另一种demosponge, Stylocordyla chupachups (Sarà et al. 2002)中进行过一次。Cárdenas等人获得的结果证实了直接、非幼虫发育作为一种单独类型的海绵胚胎发育的区别。变形是海绵发育的关键阶段之一。它需要从幼虫到成虫身体计划的根本重组。这一发育时期的标志是主体轴的重建和幼虫细胞的深刻转分化。自19世纪以来,海绵变形引起了研究人员的极大关注。其中许多研究都涉及钙质海绵的变质(Ereskovsky 2010; Cajado和Lanna,本期),因为它们是唯一有机会探索各种含水系统出现的海绵类。Lanna和Klautau首次对两种钙质海绵(syconoid Sycettusa hastifera和leuconoid pareucilla magna)在变质和含水系统发育过程中的形态发生过程进行了表征。在这两个物种中,成虫含水系统的发育都是从幼果的子囊系统开始,然后经过上皮细胞的形态发生,但类型不同。对S. hastifera和P. magna的胚胎后发育的描述将使这些物种成为未来实验研究的模型,这些实验研究不仅对Porifera的进化至关重要,而且对整个后生动物的进化也至关重要。最后,Ereskovsky和Lavrov的综述提供了海绵无性生殖模式的当前关键概述。虽然无性生殖在海绵中广泛存在,甚至在许多海绵物种中成为动物生命周期的一个组成部分,但它长期以来一直处于海绵发育研究的边缘。然而,近几十年来,一些形式的无性繁殖(淡水退海绵动物的繁殖和海洋同硬胚动物的出芽)已经成为Evo-Devo研究的有希望的模型(Funayama 2010; Okamoto等人2012;Rocher等人2024;Leys等人2025)。在他们的综述中,Ereskovsky和Lavrov总结了四类海绵不同类型无性生殖的形态发生的现有数据,并指出了海绵无性生殖未来需要研究的方面。通过这个问题,我们希望阐明海绵发育和生殖生物学的几个当前问题。我们相信这些研究和评论文章不仅会引起发育和进化生物学家的兴趣,而且会激发对这一迷人动物群体的新研究。亚历山大V.埃列斯科夫斯基:概念化,写作-原稿。安德烈·拉夫罗夫:构思,写作-原稿。数据共享不适用于本文,因为在当前研究中没有生成或分析数据集。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
CiteScore
5.20
自引率
0.00%
发文量
78
审稿时长
6-12 weeks
期刊介绍: Molecular Reproduction and Development takes an integrated, systems-biology approach to understand the dynamic continuum of cellular, reproductive, and developmental processes. This journal fosters dialogue among diverse disciplines through primary research communications and educational forums, with the philosophy that fundamental findings within the life sciences result from a convergence of disciplines. Increasingly, readers of the Journal need to be informed of diverse, yet integrated, topics impinging on their areas of interest. This requires an expansion in thinking towards non-traditional, interdisciplinary experimental design and data analysis.
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