Parallel evolution of direct development in frogs ‐ Skin and thyroid gland development in African Squeaker Frogs (Anura: Arthroleptidae: Arthroleptis)

• Published in: Developmental dynamics Vol. 250; no. 4; pp. 584 - 600
• Main Authors: Naumann, Benjamin, Schweiger, Susan, Hammel, Jörg U., Müller, Hendrik
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01.04.2021; Wiley Subscription Services, Inc
• Subjects: Animals; Anura - embryology; Arthroleptis; Biological Evolution; Cardioglossa; Constraints; developmental constraints; Epidermis - growth & development; Epidermis - metabolism; Evolution; Feeding behavior; Frogs; heterochrony; Histology; Larva - anatomy & histology; Larvae; Life history; Maturation; Metamorphosis; Metamorphosis, Biological; Morphology; Proliferating Cell Nuclear Antigen - metabolism; Skin; Skin - embryology; Skin Pigmentation; Swimming; tadpole; terrestrialization; Thyroid; Thyroid gland; Thyroid Gland - embryology; developmental constraints; tadpole; Cardioglossa; heterochrony; terrestrialization
• ISSN: 1058-8388; 1097-0177
• DOI: 10.1002/dvdy.275

Background Cases of parallel evolution offer the possibility to identify adaptive traits and to uncover developmental constraints on the evolutionary trajectories of these traits. The independent evolution of direct development from the ancestral biphasic life history in frogs is such a case of parallel evolution. In frogs, aquatic larvae (tadpoles) differ profoundly from their adult forms and exhibit a stunning diversity regarding their habitats, morphology and feeding behaviors. The transition from the tadpole to the adult is a climactic, thyroid hormone (TH)‐dependent process of profound and fast morphological rearrangement called metamorphosis. One of the organ systems that experiences the most comprehensive metamorphic rearrangements is the skin. Direct‐developing frogs lack a free‐swimming tadpole and hatch from terrestrial eggs as fully formed froglets. In the few species examined, development is characterized by the condensed and transient formation of some tadpole‐specific features and the early formation of adult‐specific features during a “cryptic” metamorphosis. Results We show that skin in direct‐developing African squeaker frogs (Arthroleptis) is also repatterned from a tadpole‐like to an adult‐like histology during a cryptic metamorphosis. This repatterning correlates with histological thyroid gland maturation. A comparison with data from the Puerto Rican coqui (Eleutherodactylus coqui) reveals that the evolution of direct development in these frogs is associated with a comparable heterochronic shift of thyroid gland maturation. Conclusion This suggests that the development of many adult features is still dependent on, and possibly constrained by, the ancestral dependency on thyroid hormone signaling. Key Findings Skin developemnt in the direct development frog genus Arthroleptis shows a larval, metamorphic and adult‐phase. Thyroid maturarion in Arthroleptis is accelerated and happens during the embryonic phase. The correlation of the accelerated developemnt of the skin and thyroid gland indicates an ancestral constraint of skin development by thyroid hormone.