Frontiers in zoology · 2026
Temporal patterns of thyroid gland maturation and skin metamorphosis in terrestrial indirect-developing de Villiers moss frogs (Arthroleptella villiersi Hewitt, 1935).
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Naumann Benjamin, Schweiger Susan, Müller Hendrik
Аннотация
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.
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.