Temporal patterns of thyroid gland maturation and skin metamorphosis in terrestrial indirect-developing de Villiers moss frogs (Arthroleptella villiersi Hewitt, 1935)

IF 2.8 2区生物学 Q1 ZOOLOGY

Frontiers in Zoology Pub Date : 2026-09-23 DOI:10.1186/s12983-026-00631-4

Benjamin Naumann,Susan Schweiger,Hendrik Müller

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引用次数: 0

Abstract

Abstract Background Anurans show diverse life histories ranging from the ancestral aquatic indirect development to derived terrestrial developmental modes that often correlate with the reduction of larval characters. The de Villiers moss frog Arthroleptella villiersi Hewitt, 1935 (Pyxicephalidae) exhibits terrestrial indirect development, hatching as endotrophic tadpoles that undergo metamorphosis within the jelly nest. We investigated the timing and histology of skin and thyroid gland development of A. villiersi to test whether metamorphic rearrangements were conserved and to assess the role of heterochrony in terrestrialization of anuran life histories. Results Histological analyses revealed a conserved sequence of thyroid maturation compared to aquatic-indirect and terrestrial direct developing anurans. Skin development recapitulates tadpole typical features, including unicellular glands, a two-layered epidermis, and neuromasts. Subsequent metamorphic rearrangements lead to a three-layered epidermis, stratum corneum, multicellular mucus and granular glands, and reorganized melanophore layers. Neuromasts appear at hatching, differentiate, and degenerate shortly before metamorphosis, correlating with thyroid maturation. Heterochrony plots revealed minor shifts in timing of skin development, including pre-displacement of the development of dermal melanophores and the post-displacement of multicellular granular glands, compared to aquatic indirect-developing anurans. Conclusions Our findings demonstrate that A. villiersi retains a conserved metamorphic remodeling of the skin that correlates with thyroid maturation. The observed minor heterochronic shifts highlight the modularity of skin development without evidence for temporal co-dissociations and therefore indicate an integrated “skin unit of evolution”. This indicates that evolutionary transitions to terrestrial life histories in anurans can occur without a fundamental reorganization of skin developmental pathways.

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陆生间接发育的德维利尔苔藓蛙甲状腺成熟和皮肤变态的时间模式（维利尔西·休伊特，1935）

Anurans的生活史多样，从原始的水生间接发育模式到衍生的陆生发育模式，往往与幼虫特征的减少有关。de Villiers苔藓蛙Arthroleptella villiersi Hewitt， 1935 （Pyxicephalidae）显示陆地间接发育，孵化为内养蝌蚪，在果冻巢内经历蜕变。我们研究了A. villersi皮肤和甲状腺发育的时间和组织学，以检验变质重排是否保守，并评估异时性在无尾猿生活史的陆地化中的作用。结果组织学分析表明，与水生间接发育和陆地直接发育的无尾猿相比，无尾猿的甲状腺成熟序列较为保守。皮肤发育再现了蝌蚪的典型特征，包括单细胞腺体、两层表皮和神经鞘。随后的变质重排形成三层表皮、角质层、多细胞粘液和颗粒腺体，以及重组的黑素细胞层。神经肥大出现于孵化、分化和变性前不久，与甲状腺成熟相关。异时性图显示，与水生动物间接发育的无尾猿相比，皮肤发育时间发生了微小的变化，包括皮肤黑色素细胞发育的前移位和多细胞颗粒腺体的后移位。结论：我们的研究结果表明，a . vilersi保留了与甲状腺成熟相关的皮肤保守的变态重塑。观察到的微小的异时性变化突出了皮肤发育的模块化，而没有时间共解离的证据，因此表明了一个完整的“皮肤进化单元”。这表明，在没有皮肤发育途径的基本重组的情况下，无尾动物的进化过渡可以发生在陆地生命史上。

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来源期刊

Frontiers in Zoology ZOOLOGY-

CiteScore

4.90

自引率

0.00%

发文量

审稿时长

>12 weeks

期刊介绍： Frontiers in Zoology is an open access, peer-reviewed online journal publishing high quality research articles and reviews on all aspects of animal life. As a biological discipline, zoology has one of the longest histories. Today it occasionally appears as though, due to the rapid expansion of life sciences, zoology has been replaced by more or less independent sub-disciplines amongst which exchange is often sparse. However, the recent advance of molecular methodology into "classical" fields of biology, and the development of theories that can explain phenomena on different levels of organisation, has led to a re-integration of zoological disciplines promoting a broader than usual approach to zoological questions. Zoology has re-emerged as an integrative discipline encompassing the most diverse aspects of animal life, from the level of the gene to the level of the ecosystem. Frontiers in Zoology is the first open access journal focusing on zoology as a whole. It aims to represent and re-unite the various disciplines that look at animal life from different perspectives and at providing the basis for a comprehensive understanding of zoological phenomena on all levels of analysis. Frontiers in Zoology provides a unique opportunity to publish high quality research and reviews on zoological issues that will be internationally accessible to any reader at no cost. The journal was initiated and is supported by the Deutsche Zoologische Gesellschaft, one of the largest national zoological societies with more than a century-long tradition in promoting high-level zoological research.