Abstract
Direct development is a reproductive mode in amphibians that has evolved independently from the ancestral biphasic life history in at least a dozen anuran lineages. Most direct-developing frogs, including the Puerto Rican coquí, Eleutherodactylus coqui, lack a free-living aquatic larva and instead hatch from terrestrial eggs as miniature adults. Their embryonic development includes the transient formation of many larval-specific features and the formation of adult-specific features that typically form postembryonically—during metamorphosis—in indirect-developing frogs. We found that pre-hatching developmental patterns of thyroid hormone receptors alpha (thra) and beta (thrb) and deiodinases type II (dio2) and type III (dio3) mRNAs in E. coqui limb and tail are conserved relative to those seen during metamorphosis in indirect-developing frogs. Additionally, thra, thrb, and dio2 mRNAs are expressed in the limb before formation of the embryonic thyroid gland. Liquid-chromatography mass-spectrometry revealed that maternally derived thyroid hormone is present throughout early embryogenesis, including stages of digit formation that occur prior to the increase in embryonically produced thyroid hormone. Eleutherodactylus coqui embryos take up much less 3,5,3′-triiodothyronine (T3) from the environment compared with X. tropicalis tadpoles. However, E. coqui tissue explants mount robust and direct gene expression responses to exogenous T3 similar to those seen in metamorphosing species. The presence of key components of the thyroid axis in the limb and the ability of limb tissue to respond to T3 suggest that thyroid hormone-mediated limb development may begin prior to thyroid gland formation. Thyroid hormone-dependent limb development and tail resorption characteristic of metamorphosis in indirect-developing anurans are evolutionarily conserved, but they occur instead in ovo in E. coqui.
Highlights
Direct development, a distinctive life-history mode in amphibians and other animals, has evolved in anurans multiple times from the ancestral biphasic life history; it characterizes many hundreds of living species [1]
We investigated whether E. coqui tissues are capable of responding directly to T3 action by mounting gene regulation responses similar to those seen in metamorphosing species
Alignments show that the predicted protein sequence of the E. coqui TRα DNA-binding domain has 97% identity to the X. tropicalis DNA-binding domain, while the TRα ligand-binding domain shared between the predicted E. coqui and X. tropicalis sequences are 98% identical
Summary
A distinctive life-history mode in amphibians and other animals, has evolved in anurans multiple times from the ancestral biphasic life history; it characterizes many hundreds of living species [1]. Even though directdeveloping frogs typically lack both a free-living aquatic larval stage and a discrete, post-hatching metamorphosis, many species display a cryptic metamorphosis before hatching: adult-specific features, such as limbs, form precociously in the egg, and numerous tadpole-specific features are present initially but are lost [Figure 1; [2, 3]]. Because such changes in frogs with indirect development are mediated by thyroid hormone (TH), the primary regulator of metamorphosis [4], evolutionary change in thyroid axis function and timing may underlie the numerous heterochronies observed between direct-developing and indirect-developing species [5,6,7,8,9]. The presumed TH independence of the first period remains to be verified experimentally
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