Wainwright Lab

University of California, Davis

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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. 

Waiting in the weeds: the Sargassum frogfish (Histrio histrio)

This blog is cross-posted on my personal website’s blog.

This week’s blog will focus on one of the things the Wainwright Lab does best, fish suction feeding. One of the current projects in the lab is comparing the kinematics of suction feeding from a large inter-specific group of fish. To do this, we film fish feeding on various prey (mostly zebrafish) with a high-speed video camera at a 1000 frames per second. Once the sequence has been captured the videos are digitized to obtain several kinematic parameters associated with suction feeding, such as gape and jaw protrusion. A product of this research is some amazing videos of a diversity of fish using suction to subdue prey. Throughout this blog I will post some examples of the fish we have filmed. Hopefully these videos will allow you to observe not only the diversity in fish species, but also the diversity in the kinematics associated with suction feeding.

The first video comes from a fish that made its debut at UC Davis’ 97th annual Picnic Day this last Saturday. The Wainwright lab had a small demonstration for the public, showing some videos of the various fish in the lab. Also present were two charismatic frogfish on display for the public. The public got to see the live fish and their feeding kinematics in slow motion from some videos. One of the fish on display was the sargassum frogfish (Histrio histrio) of the family Antennariidae. One of the unique features of Antennariidae is that the first dorsal fin ray is modified into a lure to attract prey. These fish tend to be sit-and-wait predators so the lure helps bring in food.

The sargassum frogfish can be found in most tropical seas living among the Sargassum weeds, hence its name; often near reefs. It is the only frogfish with a swim bladder, allowing it to float among the weeds. They can reach a size of 20 cm total length (from the most anterior tip to the edge of the caudal fin); and their color patterning is a mottled greenish/brown with numerous weedy dermal appendages. This patterning allows the sargassum frogfish to blend in to the weeds waiting for unsuspecting fish or shrimp. Unlike some of the other frogfish, this species swims more in open water, and some divers have noted their ability to jump out onto the floating weeds to avoid potential threats.

In terms of their feeding, these fish are mainly sit-and-wait predators, hiding among the weeds; however they do have the ability to swim after prey.  The lure in this species is small compared to some other frogfish.  Once the prey is close enough, the frogfish initiates its strike using suction to obtain the prey. Being a sit-and-wait predator these frogfish have little to no body displacement (you can see it is not swimming to capture the prey item in the video below), but you may also notice their mouth can displace a good distance in order to capture the prey. This clip is a mid-water strike, typical of this species. These strikes are also extremely quick. This video was filmed at 1000 frames per second, but is playing back at 10 frames per second; so the actual strike is much faster than the video playback.  One of the things we are interested in is the variation in kinematics of suction feeding associated with different ecologies. Have sit-and-wait predators evolved a greater mouth displacement compared to more active foragers? The data we are collecting will be able to shed light on some of these questions, and the sargassum frogfish is a good example of a sit-and-wait predation strategy.

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!

Mysteries in Fish Functional Morphology 2. Halfbeaks

Look at the head and jaws of a halfbeak:


The lower jaw appears very elongate, reaching as much as ten times further than the upper jaw. What is the function of this bizarre anatomy? Is it used in feeding? Is it used in locomotion? If so, how?

Halfbeaks (Hemiramphidae) are related to needlefish, flying fish and sauries. They are slender-bodied fish that spend most of their time swimming right up at the surface of the water where they are expert at hiding from predators. They mainly occupy warm and temperate inshore marine habitats, though there is also a radiation of freshwater forms. The marine species feed on drifting pieces of plants and zooplankton. The freshwater species and most inshore marine forms also eat drifting surface insects.

Once you get past the very strange appearance of these fish and closely inspect the head you find that the long lower jaw is not actually a lower jaw but instead an absurdly long chin (have a look at the diagrams below from Montgomery & Saunders 1985). The toothed lower jaw is short and matches the toothed upper jaw. The halfbeak is actually a very long extension of the part of the mandible that is below, and in front of the teeth – a chin. The structure is smooth and not armed with teeth. This is our first clue that the structure is not an elaborate jaw used in prey capture. If it’s not part of the feeding apparatus, then how does it function?


One idea that has some support is that the long chin is part of a specialized sensory devise. Montgomery & Saunders (1985a) showed that there are a series of lateral line pores along the length of the lower jaw, with neuromasts in between these pores. They argued that this long structure, equipped with the lateral line pits, may function in prey detection. The species they worked with feeds at night on large zooplankton and they showed it is capable of detecting live plankton in total darkness. In effect, they argue that the halfbeak functions as an extension of the lateral line system that may aid these fish in nocturnal attempts to locate moving prey animals in midwater habitats.

This is a fascinating proposal that may help us understand the function and evolution of the halfbeak. But the system requires more attention before we fully understand how it works and how it evolved. It would be valuable to model the potential sensory advantage of the long, sensitive chin. Does it convey a major performance advantage over fish that lack such a device? What was the evolutionary sequence here? Did the long chin evolve as a specialization of the lateral line system, or did the long chin evolve first for a different function, and then become co-opted for use as a scaffolding for the sensory system? And, what role does the long lower jaw play during prey capture? Such a large structure must interact with prey during feeding. Are there other, secondary functions of the long chin? What do you think?

Montgomery, J.C. & A.J. Saunders. 1985. Functional morphology of the piper Hyporhamphus ihi with reference to the role of the lateral line in feeding. Proc. Roy. Soc. Ser. B. 224:197.

Saunders, A.J. & J.C. Montgomery. 1985. Field and laboratory studies of the feeding behavior of the piper Hyporhamphus ihi with reference to the role of the lateral line in feeding. Proc. Roy. Soc. Ser. B. 224:209.

Modeling the distribution of sasquatch – the first published study using ENMTools

Lozier, Aniello, and Hickerson just published a paper in the Journal of Biogeography in which they use sasquatch sightings and footprints to model the distribution of this elusive imaginary species. They went one step further and modeled the effects of climate change on sasquatch distributions, showing that our furry friends are only going to become more elusive with time. Finally, they used ENMTools to demonstrate that sasquatch distributions were statistically indistinguishable from those of the black bear, suggesting that many of the bigfoot sightings may have been a case of mistaken identity.

Just to put a punchline on the whole thing, the public response to the New Scientist article about the study has led to a rush of public comments claiming that the study is biased due to the a priori assumption that sasquatch isn’t real.

Stickleblog: 80s stickleback (but without the crazy hair)

ResearchBlogging.orgBack in the early 80s, Don McPhail worked on sticklebacks in Vancouver Island, and specifically in some intriguing lakes that had not one but two different species of sticklebacks in them. Ten years later, McPhail and Schluter would build on this research and help to catapult stickleback to the forefront of evolutionary biology.

But for now, let’s go back to the 80s and look at a little paper with big implications.

The Enos Lake stickleback species pair consisted of a benthic species and a limnetic species, though they are sadly no longer with us due to an invasive species introduction. As is generally the case with these species pairs, benthics are larger, with deep bodies and small short gill rakers, whereas limnetics are smaller with slim bodies and lots of long filamentous gill rakers.

However, morphological differences do not necessarily translate into ecological differences, so the authors tested the performance of the different species on its preferred habitat. Three experiments were performed: a prey size trial, a feeding trial on benthic substrate, and a plankton feeding trial.

In the size trial, benthics ate significantly larger prey than either limnetics or hybrids between the two forms. In the feeding trial on the benthic substrate, limnetics and benthics made similar numbers of strikes, but benthics were significantly more successful at capturing prey. In the zooplankton trial, the stomachs of limnetic stickleback contained a much higher number of prey items than than the stomachs of benthic stickleback.

The performance data from these three experiments supports the hypothesis that the Enos Lake stickleback pair does have ecological as well as morphological differentiation, though there are some interesting issues with limnetic stickleback in particular. When the authors allowed female limnetics to feed on the benthic substrate, the sticklebacks did not, though male limnetics fed freely, and made just as many feeding strikes as benthics of both sexes.

A possible reason might be that male limnetic stickleback have to spend time near the benthos to construct their nests, so it would make sense to eat benthic prey items, whereas a female only has to approach the benthos to find a suitable male, and can spend the rest of her time in the water column eating zooplankton.

When Stickleblog returns, we’ll continue our look into the species pairs with a Schluter paper that examines hybrid performance relative to limnetics and benthics.

P. Bentzen, & J. D. McPhail (1984). Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair Can. J. Zool, 62 (11), 2280-2286 DOI: 10.1139/CJZ-62-11-2280

Catch Peter on National Geographic TV tonight!

If you’re quick you might be able to catch Peter on National Geographic TV tonight on the show “Hooked On Fish”. It’s a great show, using stories of anglers catching huge fish as a jumping-off point to talk about some fascinating natural history and conservation issues.

If you’re not fast enough to see it on the air tonight, you can at least get a sample of it here.

Stickleblog: Caught in the act

ResearchBlogging.orgThis week, I’m going to discuss a cool paper that came out of Dolph Schluter’s lab in 2008. The paper zooms in on a particularly interesting part of stickleback evolution, the transition between an ancestral marine form that breeds in fresh water to a population that lives in freshwater year-round.

Usually, (and this is one of the “color-coded for your convenience” things that make stickleback a fantastic model system) you can get a good idea where a stickleback is from by looking at its armor plates. Stickleback from marine habitats tend to have a full complement of plates, whereas sticklebacks from freshwater habitats will have few to no plates:


Stickleback armor plate phenotypes: fully plated (top), partially plated(middle), low plated(bottom)

The authors sorted through hundreds of marine stickleback to find fish that had intermediate numbers of plates, which signified that they were heterozygotes for the gene that governs plate number, Eda. These fish were placed in experimental ponds and allowed to breed. Because the fish were heterozygotes for Eda, they produced offspring with high, medium, and low plates, which gave the authors a chance to observe if natural selection favored the low-plated form in freshwater.

In each pond, the frequency of the low allele increased over time, and in a similar way. There was a slight dip when fish were very young, but then frequency increased until the fish reached breeding condition. Interestingly, fish carrying the low allele grew faster and reached breeding condition sooner than fish carrying the high allele, probably because building armor plates takes energy that could be spent on growing more quickly.

The story is more complicated than that, though – not only is there a period early in life where the high allele appears to be favored, but there is also a point where fish with intermediate plates have the highest fitness, which is difficult to explain. The authors raise the possibility that the Eda gene that controls plates in stickleback may affect other traits (pleiotropy). Either way, it looks like even the most well-understood stickleback phenotype has more to tell us.

Barrett, R., Rogers, S., & Schluter, D. (2008). Natural Selection on a Major Armor Gene in Threespine Stickleback Science, 322 (5899), 255-257 DOI: 10.1126/science.1159978

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