University of California, Davis

Category: vision

The eyes of reef fishes

[cross-posted on my personal blog, as well]

Peter and I recently published a paper in BMC Evolutionary Biology and today the final HTML and PDF versions have become available. BMC is an open access journal, so everyone can read the paper:

Schmitz, L. & P.C. Wainwright (2011). Nocturnality constrains morphological and functional diversity in the eyes of reef fishes. BMC Evolutionary Biology, 11: 338. html, reprint.

We have several really interesting results. The eye morphology of nocturnal reef teleosts is characterized by a syndrome that indicates good light sensitivity. Nocturnal fishes have large relative eye size, high optical ratio and large, rounded pupils. However, there is a trade-off. Improved optical light sensitivity comes at the cost of reduced depth of focus and reduction of potential accommodative lens movement. Diurnal reef fishes, which are released from the stringent functional requirements of vision in dim light, have much higher morphological and optical diversity than nocturnal species. Diurnal fishes have large ranges of optical ratio, depth of focus, and lens accommodation.

This paper is the first outcome of the analysis of a data set on the eye morphology of 265 species in 43 families of teleost reef fishes. It’s an enormous amount of data. All in all, we measured 5 traits in both eyes of 849 specimens, resulting in one of the largest data sets on eye morphology ever assembled. One aspect I would like to stress is that we measured eye morphology on fresh fish (in accordance to the UC Davis animal care protocol). The fixation process that preserved specimens went through may have altered eye morphology, so we wanted to avoid this potential problem.

I also would like to highlight one of the analyses in our paper. We assessed morphological diversity of diurnal and nocturnal species by calculating the combined variance of all shape axes of a principal component analysis. However, there are far more diurnal (n=211) than nocturnal species (n=54) in the data set, and ultimately the results may be biased because of uneven sampling. Inspired by a suggestion from David Bellwood we designed a simple rarefaction analysis. We randomly re-sampled 54 diurnal species (matching the number of nocturnal species) without replacement and calculated variance on PCs 2-5, and repeated this procedure 100, 000 times. This resulted in 100,000 PC analyses with the same number of diurnal and nocturnal species, with diurnal species randomly selected anew for each run. Then, we compared the distribution of nocturnal variances to the bootstrap distribution of diurnal variances. The results are convincing and, importantly, should no longer be biased by uneven sampling. The rarefaction is easily done in ‘R’; let me know if you are interested in the code.

Finally, here are thumbnails of all figures in the paper, with links to the corresponding to the high-resolution files. Feel free to use for teaching purposes.

Bigger eyes at high latitudes

There is a

growing body of evidence that light levels have a profound effect on the evolution of eyes. Most of these studies deal with comparisons between different species, but now there is a new intriguing twist to the story. In a paper recently published in Biology Letters, Eiluned Pearce and her PhD supervisor Robin Dunbar present data indicating that light levels drive intraspecific variation in visual system size among human populations.

Pearce and Dunbar found a positive correlation between absolute geographic latitude and the size of the eye socket (orbita) and brain cavity in humans. Museum collections house a large number of human skulls with known geographic origin [assuming modern migration can be excluded; the study does not provide the historic age of the skulls], and this came in quite handy for the purpose of this study. Pearce and Dunbar quantified eye size by filling the eye socket with small glass pearls and measuring volume in graduated cylinders, which should be a pretty good proxy of eye volume. Brain cavity was filled with wax beads, instead. To account for scaling effects, they measured the size of the foramen magnum (that’s the large, round skull opening at the base of the skull), a well-supported proxy for body mass in humans. All in all, Pearce and Dunbar measured skulls from 12 different populations (55 skulls total), with a good range of geographic latitudes (1-64deg).

One might think that the correlation between latitude and visual system size may be partially driven by shared ancestry of populations, because many of the high latitude populations have small genetic distances. However, this is apparently not the case: a phylogenetically informed linear model yielded equivalent results.

So, why do human populations at high absolute latitudes have larger eyes? Well, it may indeed be related to light levels. Illumination and day length decrease with an increase in absolute latitude, which means that populations in the far North and South are exposed to lower light levels. And large eye size may improve light sensitivity. Let’s focus on this in more detail.

A large eye can have a larger optical aperture (pupil), i.e., more light can enter the eye chamber. However, the higher number of photons entering the eye does not necessarily result in better light sensitivity, somewhat in contrast to what Pearce and Dunbar say. The light-gathering capacity of an eye also depends on the size of the retinal image, or, the size of the area over which the photons are spread out or distributed. As a larger eye can also have a longer focal length, the retinal image will be larger, as well.

Physiological optics provides simple equations that help to predict how to optimize sensitivity. For example, light sensitivity to extended sources is approximated by means of the f-number (focal length/aperture diameter) or the optical ratio (aperture/[retinal diameter x focal length]). Both proxies are ratios and hence they are independent of eye size. It’s the relative size of the aperture that matters.

However, there is another possible mechanism to improve light sensitivity. The optical system is obviously only one part of the visual system. Another pathway is to increase summation, or the convergence of photoreceptors on ganglion cells. Summation increases light gathering capacity at the cost of visual acuity. So, how does visual acuity compare among different populations? Visual acuity can be approximated by the ratio of focal length/ganglion cell density. If the degree of summation, i.e., density of ganglion cell does not vary among populations then populations with large eyes should have better acuity. Intriguingly, this is not the case as Pearce and Dunbar show, which strongly suggests that populations at high latitudes have higher summation and, accordingly, better light sensitivity.

It is possible that the requirement to maintain good visual acuity at lower light levels drives the evolution of larger eyes in high-latitude populations. Thanks for a great article, and I hope that many of you will now get the calipers (glass pearls, laser-scanners, you name it) out and measure eye size in non-human subjects.

An optical illusion?

Zooplanktivory is one of the most distinct feeding niches in coral reef fish and many morphological traits have been interpreted as adaptations to feeding on plankton in the water column above the reef. One of these traditional hypotheses is that zooplanktivorous fish have larger eyes for sharper visual acuity. A larger eye usually has a longer focal length and thus is expected to produce a better-resolved image.

Peter and I tested this hypothesis with a data set on eye morphology of labrids (wrasses and parrot fishes):

Schmitz, L. & P.C. Wainwright (2011). Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes. Coral Reefs, 30: 415-428. reprint.

Labrids are a species-rich clade of reef fish with enormous morphological and ecological diversity. We sampled a total of 21 species, with three independent origins of zooplanktivory: Clepticus parrae, the Creole Wrasse (photo: fishbase.org), Halichoeres pictus, the Rainbow Wrasse (photo: wetwebmedia.com), and Cirrhilabrus solorensis, the Red-eyed Fairy Wrasse (photo: fishbase.org).

To our surprise we failed to find any indication of larger eyes in zooplanktivores. We tried several methods, including phylogenetic residuals of eye diameter on body mass and evolutionary changes in eye size along branches leading to zooplanktivores, but zooplanktivorous labrids did not show any signs of having larger eyes than other trophic specialists. Instead, we suspect that the notion of large eyes in zooplanktivorous labrids is an optical illusion evoked by a size reduction of the anterior facial region, which makes the eye look bigger.

However, we did find other features interpreted as adaptations to zooplanktivory in labrids. Both Clepticus parrae and Halichoeres pictus have a large lens for given axial length of the eye, related to better visual acuity, a round pupil, possibly an adaptation to search a three-dimensional body of water for food, and longer gill rakers to help retain captured prey.

Our results are quite interesting in that they highlight the importance of many-to-one-mapping in form-function relations. There often is more than one possible pathway to perform a function. In labrids, increase in eye size to improve visual acuity apparently is not part of the evolutionary response. But, let’s see what we can find in other groups!

Nocturnal dinosaurs

Yet another non-teleost blog, but an interesting example of functional morphology and phylogenetic comparative methods. I’m cross-posting this on my own blog, too.

Nocturnal dinosaurs. Wait a second! Is that right? Nocturnal (= night-active) dinosaurs? Yes, indeed. Contrary to what was commonly believed, many dinosaurs were nocturnal.  We have to change our perception of the dinosaur era.

All details about methods, results, and implications can be found in these two siblings papers in Science and Evolution (thanks to AAAS and Wiley for being so extremely helpful in coordinating this release!):

L. Schmitz, R. Motani, Nocturnality in dinosaurs inferred from scleral ring and orbit morphology. Science, published online 14 April 2011 (10.1126/science.1200043)

R. Motani, L. Schmitz, Phylogenetic versus functional signals in the evolution of form-function relationships in terrestrial vision. Evolution, published online 14 April 2011 (10.1111/j.1558-5646.2011.01271)

We make several important points in these papers: (i) Dinosaurs were not restricted to day-activity (diurnality) by any means, (ii) Activity patterns evolve following ecological characteristics (e.g., diet+body size, terrestrial or flying), (iii) Physics of the environment drive the evolution of shape, (iv) We have a great new tool for reconstructing ecology of extinct species.

So, why did everyone think that dinosaurs were diurnal in the first place? We think there are at least two (historical) reasons. First, several decades ago dinosaurs were portrayed as sluggish, “cold-blooded” animals. It seemed too unlikely that these animals were capable of being active at night, when ambient temperatures were cold compared to the day. Second, the idea of diurnal dinosaurs may have arisen because many (paleo)biologists were trying to explain why the majority of mammals is nocturnal – and the picture of dinosaurs occupying the diurnal niche, pushing the mammals into the dark just seemed to fit all too well.

Well, that story isn’t all that simple and straight-forward anymore. Dinosaurs were nocturnal, too. And we don’t even know if the earliest mammals were actually nocturnal (Kenneth Angielczyk at the Field Museum and I are working on this right now). So, the assumed split in activity pattern between mammals and dinosaurs is certainly rejected. However, we do see a different pattern emerging. It appears as if the evolution of activity patterns is driven by ecology.

We found striking similarities between the Mesozoic and today’s biosphere. Large herbivores, just like living ‘megaherbivores’, were active both day and night, probably because of foraging needs (they just had to eat most of the time…), except for the hottest hours of the day when there was risk  of overheating.  Small carnivores such as Velociraptor were nocturnal hunters. Flying species, including early birds and pterosaurs (like Scaphognathus above, with scleral ring highlighted in blue color) were mostly day-active (although some of the pterosaurs were actually nocturnal). These ecological patterns are also found among today’s living mammals, lizards, and birds.

So, how can we tell? Eye shape is the key. Nocturnal animals roam around in low light during the night, and their eyes show characteristics that relate to improved light sensitivity. Eye soft-tissues rarely if ever fossilize, but many vertebrates (e.g., teleost fish, lizards, and birds) have an extra bone element within their eyes, the so called scleral ring. Notably, neither mammals, crocodiles, nor snakes have scleral rings [for more details I would refer you to the work of Tamara Franz-Odendaal]. The scleral ring, however, is present in basal archosaurs, pterosaurs, and dinosaurs, which enables us to reconstruct eye shape in these fossils..

If you look at a bird eye (photos below) you will see the pupil opening defined by the iris. The scleral ring, situated within the sclera, the ‘leathery’ layer of the eye, surrounds the iris. The shape of the scleral ring and eye socket closely reflects eye shape, enabling us to distinguish nocturnal and diurnal dinosaurs.

For example, if you compare the scleral rings below, the nocturnal species on the right, a potoo, has a much larger ‘aperture’, or inner diameter than the diurnal hawk compared to eye socket size. Of course, the differences are often more subtle, so we use a Discriminant Analysis (DA) to retrieve a quantitative prediction. Prediction from a DA are rarely perfect, but overall the DA performs very well.

The relation between form and function of the eye is another convincing example how physics of the environment, that is light levels, drive the evolution of shape. However, it is not just physics that influences the evolution of shape. Shared ancestry is an important factor that may blur the form-function relation. Simply put, closely related species are expected to be more similar to each other than more distantly related species, so shape alone could potentially be misleading. With Ryosuke leading this part of the study, we solved this issue and developed a new method (implemented in ‘R’) that makes it possible to account for this phylogenetic bias. A step-by-step guide to this analysis is provided in the Supplementary Information of the paper in Science (www.sciencemag.org/cgi/content/full/science.1200043/DC1). We hope that this method will be helpful for other studies dealing with inferences of ecology from shape.

Eye shape revisited

In the anticipation of the publication of the dinosaur paper I thought it may be timely to highlight one of my latest papers. [Please note that this blog is also cross-posted on ecomorph.wordpress.com, my personal webpage].

Schmitz, L. & R. Motani (2010). Morphological differences between the eyeballs of nocturnal and diurnal amniotes revisited from optical perspectives of visual environments. Vision Research, 50: 936-946. [doi:10.1016/j.visres.2010.03.009]

This paper was one of the first steps towards inferring activity pattern in extinct dinosaurs and pterosaurs. We needed to find out whether it is possible to distinguish night-active and day-active living species before we could make any quantitative inferences in fossils. It was known previously that activity patterns indeed influence eye shape (see, for example, papers by Margaret Hall, Chris Kirk, and Callum Ross), but a reliable method to make quantitative predictions was still lacking.

Here is the short version of our approach: The eyes of land vertebrates cope with highly different light levels, largely depending on the preferred activity time of the animal. Night-active (nocturnal) species experience much lower light levels than day-active (diurnal) species. Twilight-active (crepuscular) and day-and-night-active species (cathemeral) species are exposed to both high and low light levels. The problem with low light levels is that it is very difficult to form a good image.

Overall, then, these contrasting lifestyles (and light levels) should drive the evolution of eye shape, because nocturnals need to have eyes with very good light sensitivity, whereas cathemerals and especially diurnals can optimize other aspects of vision.

We tackled this problem by applying Discriminant Analysis, focusing on features of macro-morphology that are correlated with optical function. Indeed, different activity patterns occupy distinct areas in morphospace and are identified with high accuracies (see the image to the left, modified from the Vision Res. paper). Diurnals are represented by open symbols, gray symbols are cathemerals, and black symbols are nocturnals.

The great news for paleobiology was that this method not only works with eye soft-tissue dimensions like eye diameter, axial length, or lens diameter (which rarely if ever fossilize), but also with skeletal features (i.e., size of the orbit and scleral ring) of birds. These skeletal structures are still correlated with optical function, even though their shape is influenced by other factors as well (see, for example, Schmitz 2009, J. Morph.). So, potentially one may be able to retrieve some or most of the optical information recorded in scleral ring and orbit structure… more on this next week!

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