University of California, Davis

Category: adaptation

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.

Size, Scales and Sceloporus

This weeks blog (also posted on my blog) is a departure from fish, but is about a recent paper of mine that uses phylogenetic comparative methods to test hypotheses for body size and scale evolution among Sceloporus lizards.

Oufiero, C.E.$, G.E.A. Gartner$, S.C. Adolph,  and T. Garland Jr. 2011. Latitudinal and climatic variation in scale counts and body size in Sceloporus lizards:  a phylogenetic perspective. In press  Evolution. DOI: 10.1111/j.1558-5646.2011.01405.x
$ These authors contributed equally

This summer the lab has a reading group on phylogenetic comparative methods, where we are reading through some of the classic phylogenetic papers discussing the various methods. This past week we focused our attention on phylogenetic generalized least squares methods or PGLS. This method was introduced by Grafen in 1989, and although it wasn’t initially a common phylogenetic comparative approach, has seen more use in recent years. For those not familiar with this method, it utilizes a regression approach to account for phylogenetic relationships. In this method the phylogeny is converted to a variance-covariance matrix, where the diagonals in the matrix represent the “summed length of the path from the root of the tree to the species node in question (Grafen 1992).” That is, how far each tip is from the root; in an ultrametric tree the diagonals in the variance-covariance matrix will all be the same. The off diagonals represent the “shared path length in the paths from the root to the two species (Grafen 1992)”. In other words, the off diagonals are the distance from the root to the last common ancestor for the two species. Similar to independent contrasts, this method assumes Brownian motion evolution; however, unlike independent contrasts PGLS assumes the residual traits are undergoing Brownian motion evolution, whereas independent contrasts assumes the characters themselves are undergoing Brownian motion evolution. The other main difference  in PGLS is the use of raw data instead of computing independent contrasts. In short, the PGLS approach is similar to a weighted regression, where the weighted matrix is the variance-covairnace matrix based on the phylogeny of the group, and assuming the same phylogeny will produce the same results as independent contrasts.

So what does this have to do with size, scales and Sceloporus? Well, in a recent study we used a PGLS approach to examine patterns of body size and scale evolution in relation to latitude and climate among Sceloporus lizards. Sceloporus (fence and spiny lizards) are a group of more than 90 species of lizards found from Central America up to Washington State in the U.S. Throughout their range they experience a diversity of habitats, from deserts to tropical forests to temperate forests; and have been used in many studies examining physiological ecology, life history evolution and thermal biology. In our study we used Sceloporus to test two hypotheses for the evolution of morphology. 1) Lizards  exhibit an inverse Bergmann’s Rule, with larger individuals found at lower latitudes and/or warmer climates. 2) Lizards from hotter environments will exhibit fewer and thus larger scales to aid in heat dissipation; whereas lizards from colder environments will exhibit more/smaller scales to aid in heat retention. There has been conflicting results for these hypotheses in the literature, and latitude has often been used as a proxy for climate. However, one of the unique things about our study is the incorporation of multivariate techniques to describe habitat. We use latitude as a predictor as well as climatic variables (temperatures, precipitation and a composite aridity index Q), and also utilize principal component analysis to characterize habitat. We therefore can test for specific climate predictors of these traits without assuming that higher latitudes necessarily equate to colder environments.

To test our hypotheses we gathered data on 106 species and populations of Sceloporus from the literature and museum specimens. We obtained latitude from the literature and source maps, and climate date from the International Water Management Institute’s World Water and Climate Atlas (http://www.iwmi.cgiar.org/WAtlas/Default.aspx). Using a recent phylogenetic hypothesis for Sceloporus (Wiens et al. 2010) we examined the relationship between maximum snout-vent length with latitude and 5 climatic predictors under three models of evolution (no phylogenetic relationships (OLS), Brownian motion (PGLS) and a model in which the branch lengths are transformed in an Ornstein-Uhlenbeck process (RegOU). To examine hypothesis 2 we examined a multiple regression with dorsal scale rows as the dependent, body size as a covariate and latitude or one of the 5 climatic predictors as independents. We also compared results with principal components 1-3 as predictors of dorsal scale counts.

So what did we find? First, we found that phylogenetic models (PGLS or RegOU) were always better fit than non-phylogenetic (OLS) based on likelihood ratio tests and AICc scores. We also found that as latitude increases mean and minimum temperatures decrease, as well as precipitation and aridity, but maximum temperature tends to increase. Thus, lizards from this group found at higher latitudes may be experiencing more desert like environments. 

For hypothesis 1, we found support for the inverse of Bergmann’s Rule when viewed from a climatic perspective; larger lizards were found in areas with higher maximum temperatures, but not at lower latitudes. We also found that larger lizards were found in more arid environments.

Photo copyright Mark Chappell

Our results for hypothesis 2 were a little more complex. We did not find support for the first part of hypothesis 2, lizards with fewer scales were not found in hotter environments. We did find support for the second part of hypothesis 2, lizards with more scales are found in environments with lower minimum temperatures. We also found a positive effect of latitude, and a significant negative effect of aridity (with lizards with more scales inhabiting more arid environments). Results with principal components were also consistent, with PC1  (a latitude/temperature axis) having a significant negative effect on scale count; and PC2 (a maximum temperature/precipitation axis) having a significant positive effect.

Our results suggest several things. First, latitude alone may not be an accurate description of the environment organisms face, particularly at the finer spatial scales over which an individual species may exist. Second, we found support for the inverse of Bergmann’s Rule at the inter-specific level, which has also been found to be a consistent trend intra-specifically in some ectotherms (see Ashton and Feldman 2003). Finally, our analyses suggest that both temperature and precipitation (hence aridity) are important to the evolution of scale counts in this group. These findings also suggest that scale size may be important for other physiological processes, such as evaporative water loss (lizards in more arid environments may have more/smaller scales to reduce rates of evaporation through the skin as has been suggested by Soulé and Kerfoot 1972 ). Examining the relationship of morphological traits that may function in physiological processes may provide insight into how these organisms may respond to global of climate change.

Stickleback attack (part 1)

Since our last video posting, many of the videos on our lab’s Youtube channel have gone viral. As of this blog post, the video of Inermia vitatta has accrued over 120,000 hits and has been featured on TV programs and newspaper articles around the globe. Not bad for a small fish!

[youtube=http://www.youtube.com/watch?v=psdLbN7skg4]

Today’s video features the threespine stickleback, Gasterosteus aculeatus, feeding on a cladoceran (Daphnia pulex). If you have a short attention span like me, one of the first things you’ll notice from the video is how shiny the fish is. The reflective armor plates and large spines are a clue that this is a threespine stickleback from an anadromous population. Anadromous stickleback have a life history similar to a miniature salmon – they are born in freshwater, travel to the ocean, then return to freshwater to breed. Unlike salmon, anadromous stickleback do not necessarily return to their home stream to breed. Anadromous stickleback also look very similar to each other – an Alaska anadromous fish looks very similar to a California anadromous fish.

Sometimes, these anadromous stickleback will travel to a newly-formed lake or river, and instead of returning to the ocean, some fish will stay in freshwater, founding a new population of freshwater stickleback. Over time, this freshwater population will evolve to better match its new freshwater habitat.

These anadromous and freshwater populations are one of the reasons stickleback are such a good system for studying evolutionary biology. We can study the result of rapid evolution in the freshwater populations, and then turn around and study the anadromous fish that resemble the fish that founded the freshwater population. Studying ancestral and derived populations is one of the few ways – short of a time machine – that we can learn the dynamics of adaptation in natural populations.

If we study how this anadromous stickleback captures prey, and then study how freshwater stickleback catch prey, we can learn a lot about the process of adaptation. I’ve devoted much of my PhD work to studying this system, and I’ll be talking more about it in future posts.

Inermia vittata: Camera Debut

Below is one of the first ever recorded high-speed video sequences of Inermia vittata, a zooplanktivore from the tropical western Atlantic.  We are using its first live appearance in the lab to see how the feeding kinematics of Inermia compare with that of other reef fishes.  Watch how far that upper jaw projects forward!

[youtube=http://www.youtube.com/watch?v=WOQ3US92Tt0]

One common name for this fish is the bonnetmouth, named after the appearance of the protruded mouth.  Like other reef zooplanktivores, Inermia appears qualitatively to be specialized at picking prey from the water column.  As you can see in the video, the mouth reaches forward, closing the distance to the prey while preparing to pull the prey closer with suction.

The evolutionary relationship of Inermia to other species has been tricky to resolve because it is very similar in appearance and behavior to other zooplanktivores such as fusiliers (Lutjanidae).  However, molecular analysis shows Inermia to be nested within the grunts (Haemulidae), which typically feed on benthic invertebrates.  A look at the pictures below will show how much different Inermia appears from a typical grunt and how similar it looks to the distantly-related fusilier.

boga boga bonnetmouth boga

Our new star, Inermia vittata

Doubleline fusilier

A fusilier, nested within the snappers (Lutjanidae)

French grunt

A close relative of Inermia

Why does Inermia look so different from a typical grunt, and why does it look so similar to a distantly related species?  Perhaps the feeding mechanisms captured in these videos can help to resolve this evolutionary anomaly.

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!

Explosive evolution in pupfish

Pupfish are indeed the only group of fish named after puppy dogs for their playful behavior. They’re best known for their ability to survive in extreme environments, like desert hot springs. However, for my dissertation research, I have focused on understanding their evolution and diversification.

Pupfish show a remarkable pattern of adaptive diversification: in only two small lake systems throughout their entire range, pupfishes are evolving from 50 – 130 times faster than all other pupfish species. Truly ‘explosive evolution‘ – the fastest morphological diversification rates measured so far in fishes, and one of the fastest rates documented among all organisms. Further, other pupfish groups of similar young age do not show such extreme rates.

Figure 3 in paper. The pupfish heat map. Colors indicate the rate of evolution for 16 traits relative to other pupfishes in a: Lake Chichancanab pupfishes and b: San Salvador Island pupfishes.

What is going on here? The short answer is the evolution of novel ecological niches. Cyprinodon pupfishes occur throughout the Caribbean and along the Atlantic coast from Massachusetts to Venezuela and as far inland as isolated springs in California and Mexico. Throughout their entire range, pupfishes are ecological generalists: they eat mostly algae, decaying vegetation, and whatever insects or crustaceans they can catch. Yumm! Although different species can often be distinguished by differences in male coloration, or subtle differences in body or fin shape, pupfish species on the whole are anatomically very similar, particularly in jaw shape. Further, multiple pupfish species never coexist in the same habitat.

Except in two places. These are the only two places throughout their entire range where multiple pupfish species coexist and specialize on entirely new resources. On the tiny island of San Salvador in the Bahamas (only 11 miles long!), three pupfish species coexist in the inland salty lakes. Incredibly, one of these has evolved to feed almost entirely on the scales of other pupfishes! While scale-eating has evolved at least 14 times in other groups of fishes, within the 1,500 species of atherinimorphs, to which pupfish belong, this undescribed pupfish species is the only known scale-eater! While previous researchers speculated that it may eat scales or other fish, I was stunned to find only scales and no whole fish when I began examining the guts of this species (n = 60). This behavior is easy to watch in the field – the scale-eater stalks any nearby pupfish, quickly orienting perpendicular to its prey, striking and biting off scales, then stealthily moving on to the next target, just like a pup-tiger.

Cyprinodon sp. ‘scale-eater’: Males in full breeding coloration photographed in their natural habitat on San Salvador Island.

There is a second ecologically specialized species in these San Salvador lakes. This species has shortened jaws for crushing its diet of snails and ostracods. Moreover, it has a nose! This is one of the few fish species that tucks its jaw underneath protruding nasal tissue surrounding protruding bones (maxilla and nasal) on the face of the fish.

Cyprinodon sp. ‘nose’ What looks like an upper lip in this photo is actually the fish’s nose protruding outward above the fish’s tucked upper jaw.

The function of this peculiar fish nose is so far unknown (or any fish nose, for that matter). I do have a couple guesses: perhaps it helps stabilize the fish’s jaw while crushing hard shells. Or, it may help with species recognition, as males gently nudge females when trying to entice them to spawn.

The second remarkable place for pupfish diversification is Lake Chichancanab, Mexico, a large, brackish lake in the center of the Yucatan peninsula (Chichancanab is Mayan for “little lake” or “little girl lake”, whichever you prefer). Chichancanab contained at least five coexisting species of pupfishes, including four ecological specialists. One of these, Cyprinodon maya, is the largest pupfish species known and also the only pupfish to eat other fish. A second species, Cyprinodon simus, is the second smallest pupfish species, and was observed feeding on zooplankton in large shoals in open water. Piscivory and zooplanktivory are unique pupfish niches found only in Lake Chichancanab.

Terribly, these descriptions of Chichancanab species are in past tense. In the early 1990’s, invasive African tilapia (probably Oreochromis mossambicus) were introduced to Lake Chichancanab. In addition, the native Mexican tetra, Astyanax sp., was also introduced. All specialized pupfish species promptly declined in abundance and frequency over the next 10 years. I visited the lake in 2009 and after surveying thousands and thousands of fish from several different basins of the large lake, I observed zero Cyprinodon maya and only one putative hybrid Cyprinodon simus. These specialized species are now functionally extinct in the lake. Thankfully, they have survived in home aquaria and backyard fish ponds in the US thanks to the efforts of dedicated aquarium hobbyists in the American Killifish Association. I am now maintaining these extinct-in-the-wild species in the lab as well.


Cleared and stained specimenof Cyprinodon maya (top), the only piscivore pupfish.

Cleared and stained specimen of Cyprinodon simus (bottom), the only zooplanktivore pupfish. Note the dramatic difference in the thickness of their lower and upper jaws. These specimens were collected in the wild before invasive species were introduced and generously loaned for this research by the University of Michigan Museum of Zoology.

Thus, in only two remarkable lake systems throughout their entire range, pupfish are speciating and adapting to novel trophic resources, like scales, snails, other fish, and plankton. These two groups of pupfishes also happen to be showing the fastest rates of evolution among all pupfishes. Probably not a coincidence: invasion of these novel ecological niches is driving incredible rates of morphological change, particularly in jaw shape.

It is particularly remarkable to see this pattern within pupfish, a group of fishes that has repeatedly been isolated in new, extreme environments and also probably has repeatedly adapted to these new environments. Several other groups of pupfishes were also evolving fast in my analysis – around 5 – 10 times faster than average, such as the groups containing the Devil’s Hole pupfish, a tiny species restricted to the smallest habitat of any known organism, a tiny cave shaft in Death Valley, shown here:

Devil’s Hole, Death Valley National Park, Nevada. This vertical shaft of water stays a balmy 94 degrees F year-round and divers have not yet found the bottom (at least 400 feet deep). Cyprinodon diabolis is restricted to eating scarce algae off a tiny rock shelf near the surface and its population size has fluctuated between 37 and around 400 fish.

Cyprinodon pachycephalus also belongs to a quickly evolving group. This is the pupfish species that lives and breeds in the hottest waters of any known vertebrate, 114 degrees Fahrenheit year-round!

These are incredibly extreme environments that would be expected to drive rapid rates of morphological evolution. Indeed, these species are changing quickly, but the Devil’s hole pupfish and C. pachycephalus are both generalist detritivores, just like their relatives.

However, to really see explosive evolution appears to require that pupfish start dabbling in entirely new ways of life, to go where no pupfish has ever gone before. (this wouldn’t be blogging without Star Trek!)

But, I haven’t yet fully answered the question I originally posed. Why have novel trophic niches evolved in these two places and nowhere else across their entire range? Certainly, the size of these two lakes and lack of competitors (except native mosquitofishes) plays a role. But, there may be many similar lakes with similar fish communities throughout the Caribbean. What is going on here? This remains an outstanding research question, one I am actively pursuing.

For the full story and contact information, please see the paper:

Martin and Wainwright. In press. Trophic novelty is linked to extremes rates of morphological diversification in two adaptive radiations of Cyprinodon pupfishes. Evolution. 

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.

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