Organismal transparency in glassfrogs: blood, metabolism and convergence
Glassfrogs are probably the only example of organismal transparency in a terrestrial vertebrate. These frogs are well known for the stunning transparency of their skin and muscles through which their bones and other organs are visible.
From Taboada et al. 2022, Science
Transparency is a fascinating form of camouflage that involves complex adaptations that reduce light dispersion and absorption throughout the entire animal. These adaptations include a set of specific mechanisms that facilitate the propagation of light through functional tissues. In vertebrates, one of the main obstacles to achieve transparency is our heavily pigmented oxygen transport system, that relies on the molecule hemoglobin inside red blood cells. Hemoglobin strongly absorbs blue–green light and this is why our blood is red and one of the main reasons why light cannot penetrate deep in our tissues.
We found that transparent glassfrogs overcame the challenge of reducing light absorption by hemoglobin by essentially hiding their red blood cells from view in cyclic, daily patterns.
Using photoacoustic microscopy, we found that when they're at rest -and vulnerable to predation- they filter ~90% of their red blood cells out of their blood and hide them in a mirror-coated liver. When they become active, they bring the cells back into the blood, which gives them the metabolic capacity to move around but at the cost of becoming opaque and compromising their leaf camouflage.
Interestingly, glassfrogs' ability to pack almost all of their red blood cells inside the sinusoids of the liver for long periods of time somehow avoids the creation of a blood clot in the process. Removing red blood cells from the body also indicates that glassfrogs likely exhibit depressed metabolic activity or non-oxidative metabolic processes when they sleep.
In the lab, we are interested in the biochemical and physiological mechanisms that regulate blood clotting and local anticoagulation in glassfrogs, and in the physiological mechanisms that permit dynamic metabolic changes to maintain transparency. We are also interested in the convergent mechanisms that led to transparent phenotypes across anurans (e.g. Hyperolids, Mantellids, Hylids, Centrolenids) To address these questions we implement a highly interdisciplinary approach that uses biochemical methods, quantitative transcriptomics, respirometry, and various microscopy imaging modalities in collaboration with Dr. Jesse Delia at the AMNH, Prof. Junjie Yao at Duke University, Prof. Sönke Johnsen at Duke University, Prof. Lingyan Shi at UCSD, and Prof. Alisa Wolberg at UNC.
Other mechanisms of transparency: tissues and scattering reduction
We showed that one of the key factors that control organismal transparency in glassfrogs relies on subtracting red blood cells from circulation and packing them inside the liver while the frogs sleep.
Despite being one of the most important component of organismal transparency, the minimization of light absorption by reducing the concentration of respiratory pigments is only one part of a set of complex mechanisms that facilitate light propagation through and within the frog tissues.
Transparency occurs when light is neither absorbed, nor scattered. In biology, highly scattering media become opaque quickly independently of pigments, and that is the reason why many albinos across the animal kingdom are non-transparent. Scattering disrupts light propagation, and this is notorious in media with high structural heterogeneity such as animal tissues. One way to minimize light scattering involves the minimization of mismatches in the refractive index of tissular components which are ultimately responsible for light dispersion.
In our lab we are interested in studying the ultrastructural and chemical mechanisms that create the stunning transparency of glassfrogs skin and muscles. We use a combination of imaging, biochemical, and in silico techniques to isolate structural components that minimize scattering. We are particularly interested in the search for clearing agents: substances that alter the refractive index of a medium to minimize the mismatches between the components of the tissues.