The Phenotypic Plasticity of Death Valley's Pupfish
Desert fish are revealing how the environment alters development to modify body shape and behavior
Life in a Refuge
Devil's Hole is considered the most restricted natural habitat for any vertebrate species. Perhaps it is fitting then that the fish that lives here—the Devils Hole pupfish (Cyprinodon diabolis)—is also unique among pupfishes. Devils Hole pupfish are generally no more than 20 millimeters in length. The species has an unusual shape: a large head, large eyes, a shallow body depth and the absence of pelvic fins. This morphological distinctiveness, combined with their reliance on only a single habitat, led to a certain notoriety that made the Devils Hole pupfish an exemplar for endangered-species conservation.
During the late 1960s and early 1970s, groundwater pumping for agriculture was dropping the water level in Devil's Hole and threatening to expose a shallow rock shelf that is the main spawning habitat for the species. Concerned about the pupfish, a group of academics, government employees and private citizens met in 1969 to speak to the protections needed for fauna in Devil's Hole. This group became the Desert Fishes Council, an organization dedicated to this day to the study and preservation of desert aquatic ecosystems. Following a series of legal challenges, the U.S. Supreme Court ruled in 1976 in favor of the Devils Hole pupfish by deciding that protections for the endangered pupfish include the groundwater that supplies their only habitat.
Although the Court's decision halted groundwater pumping in the vicinity of Devil's Hole, it was clear that reliance on a single habitat made the Devils Hole pupfish vulnerable to extinction. Three refuges were therefore built to establish additional populations of the species. These refuges were constructed to simulate the environment of Devil's Hole, and new populations were established by transferring pupfish from Devil's Hole to the refuges. In 1977, however, only five years after their introduction, pupfish in one of the refuges were found to differ morphologically from the Devils Hole phenotype. Refuge pupfish were larger and more deeply bodied, and had smaller head sizes than fish from Devil's Hole. In 2000, Andrew P. Martin and Jennifer L. Wilcox of the University of Colorado at Boulder found that pupfish in the other two refuges had also deviated morphologically, with 32 percent and 48 percent of fish exceeding the maximum length of pupfish in Devil's Hole.
What caused Devils Hole pupfish in the refuges to change their body shape? One possible explanation is that refuge populations evolved rapidly after their founding. Comparisons of microsatellite DNA loci in fish from Devil's Hole and the refuges by Martin and Wilcox suggested that refuge populations may have experienced founder effects or genetic drift—random genetic changes resulting from the establishment and maintenance of small populations. However, these processes do not appear to explain why the morphology of pupfish in all three refuges diverged in similar ways. Alternatively, rapid morphological change may reflect plastic responses to the novel conditions in the refuges.
Gabrielle A. Nevitt, a colleague at the University of California, Davis, and I tested this plasticity hypothesis by examining how the morphology of pupfish responds to extreme conditions. Since the Devils Hole pupfish is rare, we chose to study a closely related species, the Amargosa River pupfish, as a surrogate. Work by James E. Deacon and Carol D. James of the University of Nevada, Las Vegas, established that pupfish in Devil's Hole grow unusually slowly at the high temperature (33 degrees) and with the limited food supply in their habitat. Could that slow growth affect how pupfish develop morphologically?
For our experiments, we reared newly hatched Amargosa River pupfish under conditions that mimic those in Devil's Hole by raising temperature and restricting food rations. These rearing conditions led fish in the experiment to grow at a rate comparable to pupfish in Devil's Hole. Examination of the pupfish four months later revealed that Amargosa River pupfish reared with a slow rate of growth developed a morphology similar to pupfish in Devil's Hole. Although this experiment did not recreate the Devils Hole morphology fully, the Amargosa River pupfish retained many features of their juvenile life stage—a large head, large eyes and the absence of pelvic fins—into later life. We also found that at temperatures near those found in Devil's Hole, even slight differences in rearing temperature affected how pupfish developed morphologically.
But what physiological mechanism underlies this plastic response of morphology? One possible explanation was provided from a study of zebrafish (Danio rerio) by Donald D. Brown of the Carnegie Institution in Washington, D.C. Brown exposed larval zebrafish to goitrogens that block the production of thyroid hormones from the thyroid gland. Zebrafish exposed to goitrogens developed without pelvic fins—a morphology resembling that of pupfish in Devil's Hole. Thyroid hormones mediate the transition from larval to juvenile morphology in fish. This transition is also the period of life when pelvic fins first develop. Building on these findings, we exposed newly hatched Amargosa pupfish to goitrogens and found that these fish again developed body characteristics similar to pupfish in Devil's Hole. Curious whether pupfish with slow growth showed altered thyroid status, we also measured levels of the thyroid hormone thyroxine (T4) in the pupfish from the food-restriction experiment described above. We found that pupfish from the lowest ration treatment had lower whole-body levels of T4, supporting the hypothesis that environmentally induced changes in thyroid status mediate morphological plasticity in pupfish.
If phenotypic plasticity is indeed responsible for the different body shapes of refuge pupfish, one would expect to see key environmental differences between the refuges and Devil's Hole. Such evidence was provided recently by Michael S. Parker and Abraham P. Karam from Southern Oregon University. They conducted a thorough environmental assessment of the habitats of Devils Hole pupfish and found that the refuges are slightly lower in temperature and higher in dissolved oxygen, and they have more abundant food than Devil's Hole. Each of these environmental factors can affect the metabolism, and therefore growth, of pupfish. Taken together, these findings suggest that the unique morphology of pupfish in Devil's Hole may be due in part to paedomorphosis, where juvenile traits are retained into adulthood. Environmentally induced retention of juvenile features is not commonly associated with fish but has been documented in other taxa including amphibians inhabiting cold, high-elevation lakes. Our experiments, however, suggest that the physiology and development of the Devils Hole pupfish changed in the novel conditions of the refuges, producing the observed changes in morphology.