insect eyes at the nanoscale

  The prefix nano- is a unit of measurement that denotes one billionth; it is used to talk about very small things. If you were a billionaire, one dollar would represent your nano-wealth. If we go with the more traditional Wiki definition, a nanometer is one billionth of a meter, or the amount your fingernail grows in one second. Bottom line is nano- is small, very small. So much smaller than today’s subject, insect eyes, which we think of as being pretty small.

   Different insect groups (beetles, flies, cicadas, etc.) have different eye shapes that cover varying degrees of the insect head. This variation often reflects what is adaptive for a particular insect group; for instance, the eyes of dragonflies cover nearly 270º of their head, while those of june beetles cover less surface area.

Left: head of a dragonfly (Image credit: James Douch). Right head of a june beetle (Image credit)

   A dragonfly relies on their compound eyes to find and catch prey while flying, while the june beetle, a vegetarian, has a simpler task of locating a stationary deciduous tree for dinner. From an evolutionary perspective, the diversity of eye shapes across insect groups is not very difficult to modify because insects have compound eyes; meaning that the structure we recognize as an eye is actually comprised of many repeated units called ommatidia. Thus, to change the size of the eye evolution acts on the number of ommatidia, rather than on the size of a single organ.

A detailed illustration of a single ommatidium from Snodgrass (1935).

  

For details regarding the structure of the ommatidia I defer to the father of insect morphology, Robert Evans Snodgrass, and his Principles of Insect Morphology published in 1935. An interesting man with an inspiring career that would be worthy of revisiting in a later blog post. 

R. E. Snodgrass (Image credit)

 

   The outer layer of each ommatidium (singular) has a corneal lens, which is hypothesized to have self-cleaning, anti-fogging, and anti-reflective properties¹. Lucrative properties for humans trying to keep fog from freezing on power lines, or prevent condensation from accumulating on scuba diving and skiing masks. In order to put insect eye structure to work for us we first need to determine what the corneal lens structure looks like in insects, and then we may want to know how it has evolved along the insect phylogeny. The framework necessary for these investigations is an understanding of the anatomy of insect eyes, which we have thanks to Snodgrass and other curious-minded insect anatomists. And then we need a phylogeny, or historical perspective of insect relationships, to understand how these structures change through time. 

   In 2014, Sun and colleagues published a paper in the journal Small (not because the journal is small or publishes small science, but because it publishes science focused at the nano- and microscales) describing the development of an anti-fogging polymer inspired by the nanostructures on the corneal lens of a green bottle fly (Lucilia sericata, described by Meigen in 1826 - although there appears to be some conflict regarding whether this fly should be in the genus Lucilia or the genus Phaenicia. A fascinating story I’m sure but we will let that one go for now.). You have probably seen a green bottle fly, they look like house flies but are larger and metallic green. They coalesce around poop; horse poop, dog poop, etc., which is one of the reasons scientists chose this fly. They wanted to know how the eye remained pristine in “…dusty, miry, and moist environments” (p. 3001). The scientists put their study subjects in front of a fog machine and found that the eye was superhydrophobic and stayed dry while the rest of the body was covered in water droplets.

Figure 1 from Sun et al. (2014). Figure caption: "Microstructures of the fly compound eye and bio-inspired nanostructures. (a) optical image of a green bottle fly, Lucilia sericata, in a fogging test chamber showing the superhydrophobic and clean surface of the compound eyes, even with drops nucleated in the surrounding hairs, (b) schematic illustration of the anatomic structure of the fly compound eye, (c) low magnification SEM image of one fly compound eye, (d) high magnification SEM image of the compound eye showing the close packed ommatidium lens surface, (e) bubble-like protuberances with diameters of ∼100 nm on the surface of the ommatidium, (f) microstructure of the fly-eye bio-inspired ZnO nanostructures consisting of ommatidium-lens-like structures, and (g) a cross-sectional view of the bio-inspired nanostructures, showing similar structures to the anatomic structure of natural fly eyes."

   The key to keeping water droplets off of a surface is getting it to bead up to prevent the droplet from sticking, which facilitates motion in accordance with gravity. I think about this in relation to water droplets forming on the windshield of the fancy car of an unnamed family member versus the windshield of my 2006 Honda Civic. On fancy cars, water droplets bead up and slide off the windshield. On my car they spread out like an amoeba and the added surface area prevents them from sliding down. Same idea with the insect eye – the nanostructures on the surface of the corneal lens make it as hydrophobic as the windshield of a Tesla. When scientists looked at insect eyes at very high magnification, they found the surface is uneven and rough due to multiple layers of overlapping hexagonal nanostructures. 

 With this information in hand, Sun and colleagues used trial and error to establish a protocol to synthesize a polymer resembling the nanostructure of the fly-eye corneal lens. And, results from subsequent experimental tests using treated and untreated surfaces in a foggy room were very clear, the polymer was a success.

Figure 4d from Sun et al. (2014). Figure caption: "Dynamic anti-fogging properties of the bio-inspired nanostructures….. (d) Fogging of the samples placed at a tilting angle of 10^o, clearly showing the fog sliding off of the bio-inspired nanostructured coating, but strongly sticking onto the bare glass surface."

  But the question remains, what do these nanostructures look like in other insects? Does the corneal lens surface of cockroaches look the same as the green bottle fly? Based on some work done in the 1970’s, using the best technology at that time, Bernhard and colleagues² revealed significant variation of corneal lens structures in different insect groups. A recent follow-up analysis using newer technology supported the original finding and uncovered a shocking diversity of nanostructures. 

Figure 4 from Blagodatski et al. (2015). Figure caption: "Transformations of corneal nanopatterns. The morphogramme depicts the likely interconversions among the nanostructural patterns found in the insect class rather than phylogenetic relationships of the patterns. Primordial dimpled nanopatterns (1, here from a Forficula earwig) can transform into various maze-type nanostructures (2–4; 2 from a Pyrrhocoris firebug, 3 from a Tabanidae fly, and 4 from the butterfly Protographium asius). The latter can further transform into disordered nipples (6, here from the fruit fly Drosophila melanogaster), which can further become orderly packed (7, here from a Pterophoridae moth). Alternatively, parallel ridges (5, here from a Tipulidae fly) can evolve either from mazes or nipples. The figure is made of reconstructed 3D AFM images fused, for the sake of visualization not in exact scale, using MATLAB."

  Using a technique called atomic force microscopy, Blagodatski and colleagues (2015) documented how nanostructure diversity changes through time. So now, not only are we interested in how fly-eyes inspire anti-fogging polymer treatments, we are thinking about the evolution of the corneal lens and what it mean for insects carrying out their lives in miry environments. From the perspective of the insects, what I find interesting is that closely related groups do not necessarily have similar nanostructures. This is unusual because we typically think of close relatives resembling each other more than they resemble distant relatives – me and my dad look more alike than me and my friend’s dad, hopefully. Scientists often hypothesize that such a pattern is indicative of adaptation, rather than just inheriting what your ancestors had. It is too early to tell whether this is the case in insects. But the images are beautiful.

¹Bernhard, Miller, and MØller (1962) Function of the corneal nipplein compound eyes of insects. Acta Physiologica 58: 381-381

²Bernhard, Gemne, Sälstrom (1970)Comparative ultrastructure of corneal surface topography in insects withaspects on phylogenesis and function. Journal of Comparative Physiology A 67:1-25.