Metamorphosis: from aquatic juveniles to terrestrial adults

Here in the UK the weather has warmed up and spring has arrived. Daffodils and crocuses have bloomed, lambs have been bouncing around the fields, and tadpoles can be seen in the ponds.  The metamorphosis of tadpoles into froglets is a spectacular transformation during which almost every organ is subject to being modified, and it is this process we will be diving into in this article.

Frogs are part of the class of vertebrates called amphibians, which quite poetically means “double life” in Greek. Their larvae do not share the same environments, or at least the same resources, as the adults, and must go through a striking transformation to transition from an aquatic being to a terrestrial one.

The remodelling of the pre-existing tadpole organs includes the skin, respiratory system, brain, eyes, hematopoietic system, much of the skeleton, and more. Hormone signalling controls the growth and differentiation of new organs and cell types that did not exist in the tadpole, like the limbs, bone marrow, skin, and stomach glands, and it is this hormone signalling that we will discuss first.

The molecular cascade

Metamorphosis is closed linked to the environment, with hormone receptors and neuroendocrine signals translating environmental cues. Stress factors like a high number of tadpoles, the pond water levels or even the presence of predators, have been shown to have a big impact on the timing of metamorphosis.

Corticotropin releasing factor (CRF) is released by the hypothalamus when cues such as temperature and pond water levels are right. CRF then activates the pituitary gland to produce adrenocorticotrophic hormone (ACTH) and thyroid hormones (TH). Before we head any further down the cascade, lets discuss TH’s.

In frogs, TH’s orchestrate metamorphosis. They trigger complex cascades that target genes and cause often contradictory changes within cells and tissues – some cells react by proliferating while others apoptose and die. The first clue to the TH’s key role in controlling metamorphosis was found in the early twentieth century. After feeding them various meat and organ tissues, Gudernatch found that feeding tadpoles horse thyroid tissue prompted them to start changing. This was shown again in 1925 when Allen removed a group of tadpole’s thyroid glands, which then inhibited metamorphosis and forced them to grow into giant tadpoles.

TH’s are iodinated derivatives of the amino acid tyrosine. The thyroid produces mainly thyroxine (T4), a less active precursor hormone, which is changed into the more active form triiodothyronine (T3) by deiodinase enzymes. T3 and T4 are key players in controlling metamorphosis, so by feeding tadpoles sources of T3 and T4 or iodine you can stimulate or speed up metamorphic changes. Conversely, tadpoles with an iodine deficiency will have the same fate as those with no thyroid – giant tadpoles!

Thyroid hormones activate downstream molecular signalling by binding to specific hormone receptors, which induces the activation and transcription of target genes, thus leading to the morphological changes we will discuss later on. Corticoids are also essential for the genes to be expressed – these are produced by the adrenal glands and bind to glucocorticoid receptors (GR’s) which also bind to the DNA to activate the required genes.

Body remodelling

When TH’s peak and the specific genes become activated, the morphological changes begin. During this transitional phase, larval tissues that won’t be valuable to the developing froglet die and are reabsorbed, tissues like limbs grow and differentiate from scratch while other organs and body tissues are completely remodelled.

As the tadpole develops its organs, the need to adapt its respiration system becomes very important. Finger-like external gills develop behind their heads, increasing the amount of O2 they can absorb from the water. The mouth opens through to the gills, so the tadpoles open and close their mouths to push water through their pharynx and across the gills. At this stage, they filter feed and graze on algae and small particulates in the water.
When the tadpole develops its internal gills, a flap-like membrane covers the degenerating external gills that are reabsorbed. After undergoing the external and an internal gill phase, their respiratory system undergoes yet another change – the gills cleft close and the froglet switches to using a lung-type form of respiration. This happens when they transition from an aquatic to a terrestrial environment.

The hind legs develop from scratch quite a while before the froglets are to leave their aquatic home, with the front legs developing slightly later at the climax of metamorphosis, pushing through the opercular membrane just before the tadpoles leave the water. When the legs become functional, the tail starts to be reabsorbed into the body. TH’s cause the cells to die through a process called apoptosis and enzymes degrade the bulk of the tail.

Next, the intestine is transformed from the long, coiled tube perfect for their herbivorous diet, to a complex organ that shortens about 75% in length. It also differentiates into a stomach and small intestine, neither of which were present before. This happens simultaneously with changes in the microscopic structure of the gut as their diet changes from herbivorous to carnivorous.

The horny teeth that were used to tear up pond plants are lost as their jaw changes shape from a small oval into a wide mouth, and the fly-catching tongue muscles develop.
Their skin also undergoes a dramatic change. Tadpole skin consists of three layers and contains no glands, TH causes all three layers to replicate, forming a dermis and glands that are characteristic of the adult skin.
Tadpoles and frogs even use different globin molecules! The adult haemoglobin binds oxygen more slowly but has a greater oxygen releasing capacity at tissue levels, releasing it more quickly.

Another incredible change can be seen in their hearts. A tadpole has a two-chambered heart (there is only one atrium and one ventricle), while frogs have a three-chambered heart (with two atriums and one ventricle). In a tadpole, all the blood in their body moves into the atrium, then into the ventricle, where it is then forced into the capillary network of the gills. Here oxygen exchange can happen before the blood circulates around their body. This single-loop system is vastly different from the double-loop system frogs use. In this system the right atrium contains the deoxygenated blood while the left atrium contains the oxygenated. The first loop carries blood from the lungs to the heart for gas exchange, while the second loop carries the oxygenated blood to the rest of the body. The ventricle is not divided as it is in birds and mammals, so the body never receives fully oxygen-rich blood.

If you’re heading out this spring to spot some tadpoles, take an extra minute to appreciate all those changes that will take that little tadpole onto land 🐸

References
The Origins and Evolution of Vertebrate Metamorphosis, Vincent Laudet, Current Biology, Volume 21, Issue 18, 2011
The Frog, Its Reproduction and Development, Robers Rugh, The Blakiston Company 1951

Image credits
Common frog – Lesley Andrews
Hormone signalling diagram – The Origins and Evolution of Vertebrate Metamorphosis, Vincent Laudet, Current Biology, Volume 21, Issue 18, 2011
Frog leg development picture – Gary Nafis, http://www.californiaherps.com/
Heart diagram – Zina Deretsky, National Science Foundation

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