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

Abstract

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 tadpolespecific 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.

The Complex Bridge between Aquatic and Terrestrial Life: Skin Changes during Development of Amphibians

“…Another substantial adaptation through amphibian evolution is the change of the developmental model from the typical indirect way (with metamorphosis) to the direct way (the loss of an aquatic larval phase, i.e., development without metamorphosis), which is more suitable for a lifestyle change. It has been argued that the loss of the aquatic larval phase evolved several times independently in consistency with the patterns of parallel evolution [ 16 , 17 ].…”

“…Skin is one of the organs that has experienced the most extensive metamorphic rearrangement. This redesign is characterized by the degradation of the uppermost epidermal cells and the proliferation of forming the adult epidermis [ 17 , 20 ]. When amphibians metamorphose from tadpole to frogs, the transformation of the thin larval skin to adult multi-strata skin is one of the key alterations to adapt to the drier habitats [ 21 , 22 ] ( Figure 2 ).…”

The evolution of reproductive modes and life cycles in amphibians

“…In all three groups, transition frequencies are exceedingly asymmetrical, favouring loss of the larval stage. The ontogeny of different direct-developing lineages 56,57 may explain why so few direct-developing clades have had reversals. For example, direct-developing hemiphractid frogs have retained some biphasic embryonic features (e.g., oral structures) inside the egg 53,58 .…”

“…To understand how such seemingly complex changes in life-cycles can occur rapidly, we may need to gain a better understanding of their genomic and developmental causes. Developmental studies have found that direct development may evolve through heterochronic shifts in key developmental mechanisms, such as the shift in peak thyroid hormone levels during the embryonic period 56,61,[73][74][75] . Similarly, viviparity in Salamandra salamandra may have evolved via accelerated development and heterochrony of the feeding and digestive systems 67 .…”

Putative Immunological Functions of Inducible Skin-Associated Lymphoid Tissue in the Context of Mucosa-Associated Lymphoid Tissue

“…Tadpole skin consists of a two-cell layer of the epidermis, which is covered by a mucus layer. In contrast, after metamorphosis, a 5–7-cell layer of the mucus-covered epidermis, which is covered by a monolayer of keratinized cells, develops in adult frog skin ( 55 ). Amphibians such as frogs harbor MALT and M cells, but the latter were observed only in the non-keratinized epithelium.…”