Micro-organs make brutish crocodilians supersensitive

Crocodile close-up
People wonder how that is possible; that an animal with such a powerful jaw is able to sense how much pressure it can apply to the shell without killing the baby [...] The sensitivity of their jaws is equivalent to that of our fingertips.
Professor Michel Milinkovitch
University of Geneva biologists have found that sensory organs on the skin of crocodiles and their kin are sensitive to temperature and chemical stimuli, as well as movement…

Researchers from the Department of Genetics and Evolution at the University of Geneva published a paper in BioMed Central’s open access journal EvoDevo this week detailing the results of their investigation into the sensory organs that pepper the scaly skin of crocodilians, including true crocodiles, alligators, caimans and gharials.

Lead author Professor Michel Milinkovitch told ScienceOmega.com that it was almost by chance that he and his colleagues began to examine the function and morphology of the dome pressure receptors (DPRs) – also known as integumentary sensory organs (ISOs) – which allow this group of reptiles access to environmental stimuli in spite of their hard epidermal scales.

"We were studying the evolution of scales in reptiles, and we realised that the shape and position of scales on the faces of crocodilians was very different from other reptiles," recounted Professor Milinkovitch, who directs the Laboratory of Artificial and Natural Evolution (LANE) at the University of Geneva.

"Earlier this year, we published a study in Science in which we showed that the scales on the heads of crocodiles develop in a very different way from skin appendages on any other organism, and even from the scales on crocodiles’ bodies."

In the Nile crocodile (Crocodylus niloticus) and the gharial (Gavialis gangeticus) the so-called ‘micro-organs’ are present on both the head and body; while each body scale has one DPR, scales on the head can have as many as 12. In relatives such as the spectacled Caiman (Caiman crocodilus), ISOs are confined to the head. It was these two species which the team took as their focus in the current study.

A series of surprises
 

They were surprised to find that, although the scales on the crocodile’s body develop in the same way as other skin appendages in vertebrates (i.e., from a primordium which then undergoes differentiation), the same does not hold true for the head. There, the skin cracks randomly and forms grooves which interconnect with each other to finally form polygonal pieces of skin which – in developmental terms – are not actually scales at all.

Crocodile skin"We later found that primordia do develop on the head, but they form these little organs rather than scales," continued Professor Milinkovitch. "As a result, we were fully convinced that the ISOs would be different between the head and the body.

"However, we found that the specific development of these DPRs or ISOs occurs in exactly the same way, which was very surprising. On the head they develop in isolation before the scales are formed; on the body they develop after the scales have formed. Still, the morphology is exactly the same."

Molecular techniques were used to identify the neurons which innervate the micro-organs, and it was established that many markers typically found in different kinds of neurons were present. Closer examination turned up markers of mechano-sensation, rather unsurprisingly since ISOs have been described as mechano-sensorial in the past. However, very clear molecular markers of chemo-sensitive channels and of thermo-sensitive channels were also detected.

Scattered sensory islands
 

The team used electrophysiology, which involves recording the nervous impulse in these micro-organs upon application of different stimuli, to confirm the multi-sensorial nature of the DPRs. Sure enough; the experimental results reinforced the expectations of the molecular findings.

There is no sensory mechanism equivalent to this in any other vertebrate; in other vertebrates sensory receptors are diffused. We are able to distinguish temperature and pressure, for example, because the relevant neurons are diffusely distributed across our skin.

"In crocodiles, all of these different kinds of neurons are grouped to form a micro-organ," related Professor Milinkovitch. "The micro-organs are scattered across the skin and can be clearly seen since they are pigmented, appearing as little black dots. The rest of the skin is insensitive."

Although it is hard to be sure why crocodilians have evolved this way, Professor Milinkovitch believes that it may be down to their extremely tough, keratinised skin, which is present from birth.

"It is difficult to reconcile the presence of very tough skin and the ability to detect environmental stimuli, because there is a huge barrier between the environment and the lower layer of the skin," he said. "Each of these little organs is at the surface of the skin, which is modified so that stimuli can be transmitted to the organ."

Equivalent to fingertips
 

This sensitivity to external physical and chemical stimuli is beneficial for various reasons. Highly sensitive mechano-receptors assist crocodilians in finding prey, especially in complete darkness, but are also useful in intra-specific interactions. For instance, mother crocodiles take their eggs when the young are ready to hatch and help them out by crushing the shells with their teeth.

"People wonder how that is possible; that an animal with such a powerful jaw is able to sense how much pressure it can apply to the shell without killing the baby," remarked Professor Milinkovitch. "The answer is because they have this exquisite mechano-sensitivity since these micro-organs also exist within the jaw. The sensitivity of their jaws is equivalent to that of our fingertips."

Crocodile teeth close upInformation about temperature is incredibly important for crocodilians.

"They have to control their blood temperature quite accurately, because overheating is dangerous but if they are too cold they cannot digest or move properly," Professor Milinkovitch said. "These sensors give them a very accurate estimate of the temperature outside so they can decide whether they need to be in the water or basking in the sun."

While there is no definitive proof of what crocodilians do with the chemical information their sensory organs receive, it may be useful in determining the quality of an environment in terms of acidity, for example.

Not following the model
 

Although the future of ISO research at the LANE is undecided, Professor Milinkovitch is certain that research on non-model species there will continue.

"The scientific fields of developmental and evolutionary biology are dominated by classical models like the fruit fly and the mouse. These are fantastic tools, of course, but often people don’t realise that this gives us a very biased view of what’s going on in living beings. By looking only at these species we miss many interesting phenomena which exist in other species; in other words, the diversity of species is overlooked."

The development of the scales on the heads of crocs, for example, is a previously unknown mechanism for developing skin appendages. As the mechanical tension which causes cracking in the crocodile skin can also cause bending and bulging of the skin in other species during development, this phenomenon is probably relevant to many other groups, including humans.

"This is why we are keen to push forward the study of non-model species," Professor Milinkovitch concluded. "In my lab we are studying many different kinds of animals and reptiles for this reason."


Read the full text of the paper, Crocodylians evolved scattered multi-sensory micro-organs

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