Mutant ninja pupfish.

By Dr. Eric S. Cole

Most residents and visitors to the Turks & Caicos Islands are naturally drawn to their magnificent beaches and open waters. A few rare and restless souls explore the more remote—and perhaps less inviting— inland marine ponds. These “Anchialine” ponds are unique in that they provide refuge and habitat to a host of marine species rarely seen along the open coast or in the back-reef environment. Many of the ponds are served by now-famous underwater caverns, subterranean openings that access a labyrinth of saltwater chambers ultimately connecting many of these ponds to the sea. Evidence of such connections are the daily tides that raise and lower the inland ponds, creating currents that draw a snorkeler towards the cave entrance, or push them away. (These are easily avoided).

This saltwater (Anchialine) pond on East Caicos is surrounded by mangroves and fed by a saltwater cavern. It provides refuge and habitat to a host of marine species rarely seen along the open coast or in the back-reef environment.

Though each pond is unique—ranging from orange, hypersaline replicas of the Dead Sea to animal-rich “aquaria” full of wonderful sea life—one tiny charismatic fish seems almost ubiquitous, inhabiting even the smallest of permanent ponds. This is the “Pupfish.”

These Pupfish (Cyprinodon variegatus) are also known as “sheepshead minnows” (though any resemblance to something ovine escapes the author). As with many fish, the males are colorful and females are cryptic, camouflaged to escape notice by passing predators. Males display an inverted chevron of colorful scales on their heads, metallic silvery blue or green. Having hovered over these little charmers, I believe they exercise control over their display, “dimming” the iridescent glow when frightened and “brightening” it when all is clear. I have wondered if they erect these scales to produce their neon display, and flatten them to diminish it. The males find a special place to show their stuff (their “Lek”). A patch of algae will do. Then they turn on the charm and attempt to dazzle passing females.

Pupfish are described as detritivores, nibbling any edible organic matter (plant or animal) that falls within their reach. In my experience, they are also opportunistic piranha, not at all shy once they get used to your presence.

The ponds that decorate the Turks & Caicos as well as other islands in the Lucayan Archipelago have only been in existence for 10,000 years. Before that, much of our sea water was locked within great glacial ice masses, so that the islands were elevated on high, dry platforms flanked by steep cliffs that plunged into the ancient seas.

The island ponds we see today did not exist then. Within these recently-emerged ponds, scientists have found evidence of extraordinarily rapid evolution in everything from sea horses to pearl oysters and even our darling pupfish. Something about the relative isolation of these ponds and their highly variable conditions creates a laboratory of rapid evolution, natural experiments in accelerated adaptation.

A) This is the “wildtype” pupfish from which the mutant forms arose. B) Three new species of pupfish emerged in a geologic heartbeat. Top panel: the wildtype; middle panel: a “scale eater” with its extended jaw; bottom panel: a “snail eater” with thickened jaws.

On the neighboring Bahamian Platform, and specifically on the island of San Salvador, something remarkable has been happening to the resident pupfish. The normal pupfish (casually grazing on organic debris and algae) has radiated into a swarm of new species—a “species flock.” Three species have emerged in a geologic heartbeat, all co-existing within a few local ponds. In one, the pupfish jaws became reinforced into crushing mouthparts, and its diet expanded to include an abundance of hard-shelled crustaceans and snails (C. brontotheroides). One can imagine pupfish becoming isolated in a pond with an unusual abundance of hard-shelled prey, and perhaps a dearth of softer food. Mutations allowing these fish to exploit the resident hard-bodied prey would sweep this miniature, in-breeding population creating differences that would later, upon rejoining the broader population, maintain their isolation as separate species.  

An equally dramatic set of mutations occurred within this same species flock, transforming the common pupfish into something of a cannibal. Cyprinodon variegatus gave rise to C. desquamator, “the scale eater.” Scale eaters deserve special attention.

A) These photos depict the differences between the “wildtype” and “scale-eater’”pupfish. B) This scale-eater is attacking another pupfish. C) These illustrations compare the wildtype and scale-eater pupfish with its altered jaw.

Rather than swimming over algal beds and between mangrove roots, daintily nibbling at bits of detritus, desquamator has become an ambush, hit-and-run attack artist. Scale-eaters lie immobile in the algal beds, waiting for other fish to swim into view (a resident pupfish or mosquitofish). They move innocuously from their resting place, drift harmlessly towards their sibling species, and strike. The lower jaw seems almost disarticulated as it reaches low on the prey’s flank to carve off a mouthful of scales. Professor Chris Martin’s laboratory (U.C. Berkeley) has captured these attacks with high-speed video.

Videos of scale-eater attacks on other pupfish (from Chris Martin’s lab): 

Video (high-speed) showing jaw in slow-motion action: (Courtesy of Professor Chris Martin):

https://static-movie-usa.glencoesoftware.com/mp4/10.1242/584/f89ba747d96127161a5f3f9ac893869ab695ee48/JEB247615.MovieS1.mp4 

It must be disconcerting to be a “normal” pupfish sharing a pond with these scale-eating assault artists. One wonders how this species evolved, as there have clearly been dramatic changes in morphology as well as behavior. It may be difficult to be impressed by what seem like subtle changes in the dental work of a tiny fish. An image captured using micro-CT (a miniature version of a medical CAT scanner) has allowed scientists Drs. Chris Martin and Adam Summers to drive home the fearsome appearance of the scale-eater’s newly evolved oral armature.

This image shows a scale-eater pupfish skull face-on.

The “flock” of pupfish species that have emerged within a series of small inland ponds in The Bahamas, has launched numerous laboratory investigations while raising the possibility that rapid evolution may also be happening within the Turks & Caicos populations. The TCI has hundreds of small ponds and pools, most of them occupied by these charismatic preeners. No one has yet paid close attention to discover whether within these isolated populations there might be a similar mutant-species flock. On our next visit, my team will pay closer attention to these deceptively modest residents, looking for evolutionary innovations within this highly mutable species.The more time one spends visiting these precious habitats, the more one comes to appreciate their fragility, and the unique community of creatures that they each harbor. If these articles inspire you to explore, enter each pond gently, and if possible, without sun lotion. A long-sleeved shirt and neck gaiter provide ample protection from the sun and even a bit of warmth while swimming, and they protect the pond’s inhabitants from a noxious cloud of toxic irritants.