Physics versus biology

When I was in high school, my physics teacher drew a massive rectangle that took up almost the entire black board and proclaimed, "this is physics". He then drew a little rectangle inside the first one and proclaimed, "this is biology". The he made a tiny little smudge of chalk on one of the sides of the 'biology' rectangle and said, "this is chemistry, so you all should study physics because all the other major division of science are just sub-disciplines of physics".

Amusing as his performance was, there are many aspects of biology that cannot be directly or indirectly inferred from our understanding of physics. Notably, we would have never formulated the theory of evolution, which underpins our modern understanding of biology, if we had to rely on progress in physics alone. Clearly though, physics is important in shaping the evolution of particular traits. I've written many times about physics in biology, such as swimming in sharks (here), flight in albatross (here), the hammer strike of mantis shrimp (here) and the visual capability of giant and colossal squid (here and revisited here).

Almost all organisms that detect and use light do so in the same part of the spectrum, which is pretty much the same part of the spectrum we see in. Although many use slightly shorter wavelengths in the ultraviolet or slighter longer wavelengths in the infrared, no organisms that we know of use the huge parts of the spectrum in the radio, x-ray and gamma ray wavelengths. I've wondered why this is before, but Mathew Cobb wondered it out loud and got some interesting answers.

It's allometric, my dear Watson

Giant and colossal squid have the largest eyes of any living animals. Eyes are expensive organs to build and maintain, which led some researchers to suggest that there must be a strong evolutionary advantage for large eyes in giant squid. Using a mathematical model they found that giant squid eyes were best suited for detecting large dimly lit objects. They argued that the only stimulus that was both large enough and important enough for giant and colossal squid to detect was the light produced by bioluminescent organisms disturbed by hunting sperm whales.

A giant squid, Architeuthis dux (top), and a colossal squid, Mesonychoteuthis hamiltoni (bottom), being hauled up from the depths (images from National Geographic here and here respectively).

When I wrote about the paper, one of the criticisms I had was that the authors had failed to consider allometric scaling. Although the authors made comparisons of eye size with fish and extinct marine reptiles of similar size, they had not looked at eye size in other squid. Giant and colossal squid are the largest of all squid and their eyes could simply be large because they scaled up with their body size. I did a very crude analysis by conducting a literature search for papers that reported both eye size and body size in squid. From that I concluded that eye size was not disproportionately large relative to body size in giant and colossal squid.

Now, fortunately, nobody needs to rely on my poor-man's analysis. Schmitz et al. have published in BMC Evolutionary Biology that examines data from 87 different squid species and concludes that when allometric scaling is taken into account eye size in giant and colossal squids is not exceptional. In fact, it's pretty much exactly what you would expect if you scaled up another squid species to the same size. Indeed, there were a couple of groups, such as the bobtail squid, that had larger eyes relative to body size than the giant squid.

A regression of eye diameter on mantle length for 87 species of squid. Points for individual measurements in giant (yellow) and colossal (red) squid are shown for comparison (taken from Schmitz et al. 2013).

Further, Schmitz et al. also argue that many of the parameter values used in the original study are inappropriate. The original study based all of their optical performance calculations on the largest recorded giant squid eye diameter of 27 centimeters. But, this is problematic because the optical ability of such a large eye is likely to apply mainly to very large old squid, who are likely to have already reproduced. Eyes that only provide an advantage late in life are unlikely to contribute much to individual fitness. The original paper also probably set the values for the density and amount of light emitted from bioluminescent organisms in the deep sea too high.

When Schmitz et al. used more realistic values in the model they found that there was no unique advantage of large eyes for detecting large luminous objects, such as foraging sperm whales. Pupil sizes ranging from 2 centimeters up to the 15 centimeters used in the original model performed roughly equally well at detecting point sources and large luminous objects. Moreover, as eye size increased there was a slightly greater advantage for detecting point sources of light rather than large luminous objects. Thus, with more realistic parameter values, the conclusions of the original paper are essentially reversed.

References

Schmitz, L., Motani, R., Oufiero, C., Martin, C., McGee, M., Gamarra, A., Lee, J., & Wainwright, P. (2013). Allometry indicates giant eyes of giant squid are not exceptional BMC Evolutionary Biology, 13 (1) DOI: 10.1186/1471-2148-13-45  

Nilsson, D., Warrant, E., Johnsen, S., Hanlon, R., & Shashar, N. (2012). A Unique Advantage for Giant Eyes in Giant Squid Current Biology, 22 (8), 683-688 DOI: 10.1016/j.cub.2012.02.031

Flatfish eyes: The twice solved mystery

You know it's particularly mysterious when a puzzle stumps Charles Darwin and all the egghead evolutionary biologists that have come since. But, how both eyes of flatfish came to be on the same side of the head was such a bafflingly mysterious puzzle that it needed to be solved twice. By the same person.

The turbot, Psetta maxima (image Wikipedia)

In 2008, Matt Friedman was able to show that the transition to both eyes on the same side of the head was gradual. Now, in 2012, Matt Friedman has done it again and solved the mystery of the flatfish head by demonstrating that the transition to both eyes on the same side of the head was gradual. Or perhaps, in both instances the journalists overcooked the story and tried to make an interesting incremental step in our understanding of the evolution head asymmetry in flatfish into a revolution in understanding.

But, behind every popular science article beat-up of stumped boffins and puzzling riddles, there's usually some interesting science. And that's the case here. 

Flatfish are fascinating creatures. Adults live on the bottom, lying on one side, with both eyes gazing up from the same side of their head. At hatching, though, their larvae look unremarkable in comparison to other fish larvae. Their eyes are on opposite sides of their head and they swim vertically. But, late in their larval development one eye begins to migrate upwards and over the top of the head until it sits near the other eye.

Larval stages of the summer flounder Paralichthys dentatus. Each letter denotes a stage in development and 'early' and 'late' indicate the position withing the stage. The migrating eye is in grey. The migration begins during stage F, with the eye crossing the midline in stage H (image from Martinez & Bolker 2003).

Far from being stumped, several scientists put forward their explanations, including Darwin. Saltationists, such as Goldschmidt, saw it as evidence that some speciation events were the result of large mutations that revolutionised morphology. While others thought that the eye must have gradually migrated, as it does at the end of the larval period.

The evidence seems to have been more strongly in the gradualist camp. And not only because the new synthesis largely killed off the idea of saltation in evolution. It was already known that the more ancestral flatfish groups, such as spiny turbot and flounder, were less asymmetrical and less strongly associated with the bottom than the more derived groups, such as sole. The only thing that was lacking was truly smoking gun evidence.

Three species of flatfish. From top to bottom,  the spiny turbot, Psettodes belcheri, the flounder, Citharus linguatula, and the sole, Achirus klunzingeri. As you move top to bottom, the wandering eye moves further down the head (Pictures from FAO, via FishBase).

Enter Matt Friedman. He found several examples of fossilised flatfish species from two genra that were about 50 million years old. One genus, Amphistium, had been previously described, but had not been placed within the flatfish group. The other genus, Heteronectes, was previously undescribed. They were in the collections of European museums that, like most museums, had a heap of fossils that nobody had really looked at before. 

The two sides of the fossil fish Heteronectes chaneti. Note the eye on the left side (right hand image) is higher than the eye on the right (from Friedman 2012).

The reason that Amphistium had not been placed within the flatfish was that, although the eyes were not in symmetrical positions, the asymmetry was put down to distortion during fosilisation. Friedman was able to show in his 2008 Nature paper that the eye asymmetry was not as a result of distortion that that, therefore, Amphistium and Heteronectes were transitional between the symetrical ancestors and modern flatfish. 

A simplified phylogeny of flatfish showing the progression of eye migration over history. Next to each fish is a diagram of their skull from the left (top), top (middle) and right (bottom). The two rightmost fish are the modern genera Psettodes and Citharus, examples of which are shown above (image modified from Friedman 2008).

Interestingly, Amphistium and Heteronectes were alive at them same time as flatfish with the modern asymmetrical morphology. Which indicates that they aren't the direct ancestors of the modern flatfish and that the origins of flatfish are much older. This, in turn, suggests that the transitional morphology provided some advantages, since it persisted for so long in the presence of more modern eye arrangements.

The fossil flatfish Eobothus that was alive at about the same time as Amphistium and Heteronectes, but, like modern flatfish, had both eyes on the same side of its head (image the Fossil Forum).

How Heteronectes and Amphistium were so successful with one eye pointing at the bottom is not clear. However, extant species provide some clues. The less asymmetrical species spend more time hunting prey away from the bottom, where a downward pointing eye would be more useful. In addition, Friedman speculates in his 2008 paper that like many modern flatfish, Heteronectes and Amphistium may have used their dorsal an anal fins to lift their downwards facing eye into a position where it could be used. But, of course, all this assumes that lying on one side came before eye migration, which is not clear.

The European plaice, Pleuronectes platessa, using its dorsal and anal fins to lift itself off the bottom (image EOL).

Friedman's 2012 paper in the Journal of Vertebrate Paleontology, provides a much more detailed description of the morphology of Heteronectes. Because Heteronectes represents a transitional form, it may also share more characters with the common ancestor. The aim of the paper was, therefore, to use the described characters of Heteronectes to clarify the relationships between the flatfish and other groups of fish.

The analysis suggested that the Latids are the most closely related family of fish. But, Friedman cautions that his analysis was necessarily coarse. Some of the characters identified as uniquely shared by the Latids and Heteronectes may actually be general to a larger group of fish. And, because Friedman didn't examine other flatfish in the study (he must have another paper in the works), the characters identified in Heteronectes may not be shared with other flatfish.


So, two interesting papers. But, although we now know that evolution of the asymmetrical flatfish eye was gradual and, therefore, that transitional flatfish morphologies clearly were not useless, a lot of questions remain. For instance, we can only speculate about the selective pressures that drove eye migration and we don't yet know what the flatfish common ancestor looked like. 


References

Friedman, M. (2008). The evolutionary origin of flatfish asymmetry Nature, 454 (7201), 209-212 DOI: 10.1038/nature07108

Friedman, M. (2012). Osteology of †Heteronectes chaneti (Acanthomorpha, Pleuronectiformes), an Eocene stem flatfish, with a discussion of flatfish sister-group relationships The Journal of Vetebrate Paleontology, 32 (4), 735-756 DOI: 10.1080/02724634.2012.661352

Martinez, G. M. and Bolker, J. A. (2003). Embryonic and Larval Staging of Summer Flounder (Paralichthys dentatus) Journal of Morphology, 255, 162-176

All the better to see you with

Giant and colossal squid have bigger eyes than any other living animals. A paper published in Current Biology last month asks why it is that they do when other animals get by with smaller eyes. Intriguingly, they suggest that it might be sperm whale predation that has driven both body and eye size in these massive invertebrates. Unfortunately, I think the authors tackle the problem from and adaptationist perspective and do not give alternative hypotheses due consideration.

A kraken fights with a leviathan in a diorama at the Museum of Natural History (image Wikimedia Commons)

Eyes are metabolically expensive organs to build and to maintain. So it's interesting that they are so prevalent in the deep sea where sunlight is weak or never reaches. But, in the deep, animals and other organisms make their own light. Indeed, it has been estimated that 80 - 90% of creatures in the deep sea are bioluminescent. Clearly then, making and detecting light are important for life below the sun's influence. But, most animals get away with eyes much smaller than those of giant and colossal squid.

Generally speaking, big eyes are more sensitive and provide better spatial resolution. But, the amount of light reaching the retina is dependent on the ratio of focal length (the distance between lens and retina) and pupil diameter (camera mavens will recognise this ratio as the f/stop value). In some cases smaller eyes can be more sensitive because they have a shorter focal length. With longer focal length, larger eyes have greater acuity and can increase sensitivity by increasing pupil size.

The paper examines just how much visual performance in the sea improves with increasing eye size and what visual strategies giant eyes are best suited for. They take into account the focal length and pupil size plus a raft of other factors such as the transmission of light in water and background illumination. They find that giant eyes are best suited to detecting the distant shapes of large moving objects illuminated by small bioluminescent organisms disturbed by the object's passage.

The authors argue that the only objects that are both large enough and important enough for giant and colossal squid to detect at distance are hunting sperm whales. The bioluminesence stimulated by moving whales would allow giant and colossal squid to see them at about 120 meters away. Unfortunately for the squid, this is inside the distance at which the whales would detect them with their sonar. The authors argue, therefore, that the squid must use their ability to detect whales at this distance to prepare for a coordinated escape response.

The authors, I'm sure, would acknowledge that their study is speculative and important questions remain. For instance, the maximum recorded sprint speed of hunting whales is about  9 ms^-1, which would give a giant squid more than 10 seconds of advanced warning of a whale closing at speed. Giant and colossal squid are unlikely to be strong enough swimmers to flee beyond sonar range, leaving them the only option of evasive maneuvers. Surely smaller eyes and shorter detection distances would still leave them ample time to prepare to outmaneuver the whale.

The authors rule out the possibility that giant and colossal squid use their eyes to detect prey because huge eyes offer only marginally better performance than much smaller eyes. However, they only consider individual prey items and looking at the published studies on the diet of giant squid, many of their prey species are schooling fish (e.g. Macruronus novaezelandiae, Micromesistius poutassou and Trachurus trachurus) and squid (e.g. Nototodarus sloanii, Ommastrephes bartramii and Todarodes sagittatus). Although detecting individuals of these species might not favour the evolution of giant eyes, schools of prey could easily reach sperm whale size and would also trigger bioluminescence as they move. 

On moonless nights fishermen at the surface are able to use the pattern of bioluminesence stimulated by schools of fish to distinguish among several species. It's possible that giant and colossal squid could use patterns of bioluminescence to determine whether it's being stimulated by prey or non-prey species or, of course, a hunting whale. Longer prey detection distances would seem to be a highly advantageous trait for fueling the fast growth rate of giant squid (reaching 150 - 250 kg in about 5 years).

In making their argument that the eye size of giant and colossal squid is unusually large, the authors contrast them with several other extant whales and fish. None of these extant species, though, are visual predators that hunt at great depth. The authors do also compare to the extinct ichthyosaurs, which had eyes of similar size and were probably visual predators that hunted at depth. They suggest that this is because ichthyosaurs had a similar need to detect the bioluminesence stimulated by large moving objects, perhaps pliosaurs or other ichthyosaurs.

None of these comparisons are truly fair, even the ecologically similar ichthyosaurs, because they don't take into account allometric scaling effects. When making trait comparisons among lineages you should always examine the trait within lineages. It is entirely plausible that the eyes of giant and colossal squid are large simply because they're scaled up versions of those in species with smaller body size. The authors claim that giant and colossal squid eyes are unusually large even for squid, but the paper they cite in support of this point only examines changes in eye size in a single species as it grows.

The problem with looking at the relationship between eye size and body size within a single species of cephalopod is that eye size as a proportion of body size decreases as they age. This is almost certainly not e case when you examine the relationship between body size and eye size among species. As in cephalopods, eye size in vertebrates generally decreases as a proportion of body size as individuals grow. But, eye size increases as you move from species with smaller body size to species with larger body size. Unfortunately, no such among species relationship has been published for cephalopods.

In a crude attempt to get an idea of the scaling relationship in squid, I searched the literature for reports of eye size that could be linked to a length measurement. I was able to find data in three species (Dosidicus gigas, Loligo opalescens and Illex illecebrosus), but eye size as a proportion of mantel length in giant and colossal squid was within the range of these species. Although my "analysis" should be taken with some salt (e.g. some values were estimated from graphs), it seems that giant and colossal squid eyes are not unusually large when their body size is taken into account.

Although I have strong doubts that the eyes of giant and colossal squid were selected for detecting hunting sperm whales, this study does provide some interesting information about the performance of eyes in the sea. Because deep-sea squid and their predators are so hard to observe, we really only have recourse to mathematical models to determine the selective pressures on predators and prey. But, we should never ever start with the assumption that the trait of interest is adaptive and then look for explanations.

Nilsson, D., Warrant, E., Johnsen, S., Hanlon, R., & Shashar, N. (2012). A Unique Advantage for Giant Eyes in Giant Squid Current Biology, 22 (8), 683-688 

DOI: 10.1016/j.cub.2012.02.031

Anomalocaris had excellent vision

Anomalocaris is a strange and interesting genus. So strange, in fact, that three separate parts of their fossils were once identified as three separate creatures. It took nearly a century from the discovery of the first piece, for Anomalocaris canadensis to be properly identified and unified into single animal¹.

Anomalocaridids, the group in which Anomalocaris belongs, grew to over a meter in length. Although small in comparison to marine animals today, at the time they swam the oceans (see an animation), between 540 and 472 million years ago, they were the biggest predators in the sea by far^1,2.

Anomalocaridids had two segmented tentacle-like appendages that were probably used in hunting, perhaps by stabbing or by grasping prey. Their mouth was circular and had ‘teeth’ that closed like a camera shutter. Some of them may have eaten hard-bodied animals like trilobites, but it is thought that soft-bodied animals were their primary prey.