The Phenotypic Plasticity of Death Valley's Pupfish
Desert fish are revealing how the environment alters development to modify body shape and behavior
Plasticity and Environmental Change
When I first began studying the behavior of Death Valley's pupfishes, it quickly became apparent that pupfish behavior is strongly dependent on the current physical and social conditions of their habitat. I observed that male pupfish in the Amargosa River are aggressive as they protect breeding territories during early spring. Yet during summer, males abandon these territories when desiccation and an abundance of young pupfish spawned that spring makes the density of fish too high to defend territories successfully. Instead, male pupfish reduce their aggression and spend more time courting females as part of mixed-sex schools.
It was clear to me from these early observations that if I wanted to understand how Death Valley's pupfishes are evolving in their distinct habitats, I needed to examine the phenotypic plasticity of pupfish and ask how plasticity itself varies among populations living in dissimilar habitats.
The environment that organisms experience during development has long been known to affect the phenotype that they express later in life. Since phenotypic variation caused by such plasticity is environmentally generated, for many years such variation was considered to be "non-genetic" and irrelevant to evolution. Recently, however, accumulating evidence has established that plasticity itself has a genetic basis. Although the phenotypes generated by plasticity are induced by the environment, the phenotypic responses are produced by changes in gene expression. Studies have demonstrated that the sensitivity of genes responding to the environment can vary among organisms with different genetic backgrounds. The picture that is emerging suggests that the degree of plasticity an individual shows is determined both by the environment that the individual experiences and by the genomic composition of that individual.
Now that plasticity is known to have a genetic basis, and is therefore heritable, the role of plasticity in the evolution of species is being reconsidered. Mary Jane West-Eberhard of the Smithsonian Tropical Research Institute has pointed to one scenario whereby plasticity may lead to evolutionary divergence:
The origin of a new direction of adaptive evolution starts with a population of variably responsive, developmentally plastic organisms. That is, before the advent of a novel trait, there is a population of individuals that are already variable, and differentially responsive, or capable of producing phenotypic variants under the influence of new inputs from the genome and the environment. Variability in responsiveness is due partly to genetic variation and partly to variations in the developmental plasticity of phenotype structure, physiology, and behavior that arise during development. . . .
If the environment changes, plasticity may cause a reorganization of phenotype, ultimately leading to the expression of new traits in the population. If individuals in the population vary in plasticity, any resulting phenotypic differences might produce dissimilarities in reproductive success or survival that, over time, lead to evolutionary change in the population.
But how might phenotypic plasticity play a role in the evolution of Death Valley's pupfishes? To answer this question, I needed to examine the proximate mechanisms of plasticity in pupfish and explore whether those mechanisms are evolving between populations isolated in ecologically dissimilar habitats. I began my own studies by focusing on the hormonal mechanisms of plasticity. As chemical messengers, hormones influence phenotypic development by regulating gene expression in response to changes in the environment. Broadly, hormones can be viewed as a developmental link between an organism's genes and its environment.
My research on the endocrine bases of plasticity in pupfish is following two paths. In one line of study, I am asking how habitat conditions influence the morphology, or body size and shape, of pupfish. I do this by examining how environment and hormones interact in regulating morphological plasticity. As a second avenue of research, I am examining the neuroendocrine basis for population differences in aggressive behaviors. Together, these studies are uncovering how the environment experienced during early life can be important for shaping patterns of morphological and behavioral diversity in the wild.