If you think your pubescent years were incommodious, you should talk to a frog. We humans see some changes here and there, sure. But for a tadpole metamorphosing into a frog, so many profound changes occur that, were it not known to science, this developmental process would probably defy belief. It has not escaped the notice of Robert Denver, however, a developmental neuro-endocrinologist at the University of Michigan, USA. He and his team recently turned their attention to the many changes that occur in the anuran digestive system during the transition from tadpole to frog. While these changes may be less familiar than the gross anatomical changes that occur during metamorphosis, they are no less extraordinary, and they impact the animal at various levels of organization.

Underlying these changes are the anuran's evolving culinary preferences, from vegan tadpole to carnivorous frog. A taste for hemolymph requires different gastrointestinal architecture, and the frog remodels during metamorphosis by shortening the intestines and overhauling the epithelial lining. Remodeling in this way requires a halt to feeding, and what intrigued Denver and his colleagues were the signals that trigger this halt and how they may change with development.

Using Xenopus laevis as their representative anuran, the team first confirmed that food intake increased steadily throughout tadpole development before falling precipitously at metamorphic climax. The point in development at which this occurred coincided with a shortening of the intestines and an emptying of the intestinal contents, supporting the idea that feeding is arrested to enable gastrointestinal remodeling. The team then pursued the hypothesized involvement of leptin, which is the body's primary satiety hormone that makes frogs (and us) feel full. They searched for both leptin and the leptin receptor throughout the tadpole's development, finding that that initial appearance of the hormone and receptor occurred slightly out of step with each other: leptin levels increased just prior to metamorphosis, while hypothalamic leptin receptors (and their functionality) increased at metamorphic climax.

Denver and his colleagues further investigated leptin functionality by manipulating their frogs in two ways. First, the team injected pre-metamorphic tadpoles with recombinant frog leptin, finding it did not suppress feeding until just prior to metamorphic climax. Next, the investigators neutralized the leptin of tadpoles just before metamorphic climax, and found that the lack of functional leptin caused the tadpoles to resume feeding when they would normally cease.

Together, the team's results revealed two things. First, pre-metamorphic tadpoles lack central feeding control. This allows them to eat insatiably and maximize growth rate, which is important because metamorphosis from a highly vulnerable tadpole into a less vulnerable frog occurs only once sufficient weight has been packed on. Second, leptin's role evolves throughout development. Initially, leptin functions as an adiposity signal to the hypothalamus, effectively telling it that the body is ready for the hypothalamus to begin secreting metamorphosis-inducing hormones. As metamorphosis progresses, the hypothalamus eventually produces leptin receptors, which, by metamorphic climax, alter leptin function from adiposity signal to appetite suppressant. With feeding halted and the intestines emptied of their contents, the gastrointestinal tract is free to remodel for its upcoming carnivorous diet.

In the wild, Xenopus parents hit the road immediately after the female lays her hundreds of fertilized eggs. Most humans would probably frown upon this hands-off parental approach, but I implore those humans to recall their own pubescent years – better yet, those of their children should they have any – and then ponder the many-fold greater hormone-driven changes that occur during anuran development. Now multiply that by several hundred offspring. Still frowning?

References

Melissa
Cui Bender
,
Caroline
Hu
,
Chris
Pelletier
and
Robert
J. Denver
. (
2018
).
To eat or not to eat: ontogeny of hypothalamic feeding controls and a role for leptin in modulating life-history transition in amphibian tadpoles
.
Proc. R. Soc. B, 
285
,
20172784
.