The interpretation of genes: the "expression" of a genome is best understood as a dialogue with an organism's environment. That dialogue, not the genes alone, determines which ant becomes a queen, which fish becomes a male

We sometimes think of the environment as "out there," a place separate from us, a place we can enter and leave at will. But the environment is, quite simply, the context for all of life; it is what makes us what we are. Plants in dry soil grow deeper roots than those in wet soil. Turtle eggs become male or female depending on temperature. A fish may become female in one social environment, male in another. Genes not only direct, they also take orders. In a sense, our genes are the means by which the environment regulates our development.

Everything about us--from the shape of a toe to the shape of a protein, from the year we enter puberty to the amount of stress hormone we release when another car gets our parking space--is a manifestation of an ongoing conversation between genome and environment. This conversation started billions of years ago, when life began, and goes on every minute of our lives. Yet, strangely, it's a conversation to which most biologists turned a deaf ear for decades, starting in the 1940s, when the focus of biological research became overwhelmingly genetic. We've all read or been told repeatedly that genes provide a "blueprint" for the body, that genes "program" development, that we are "products of our genes." A 1996 introductory biology text used by more than half of all college biology majors in the United States asserts: "An organism's development is largely determined by the genome of [the fertilized egg] and the organization of the cytoplasm of the egg cell." No mention is made of any influences outside the egg.

How did biologists come to snub so thoroughly one partner in the developmental conversation? The answers lie deep in the political and scientific history of biology. Decades before the advent of genetics in 1900, biologists sought to understand heredity by studying development, the process by which organisms take shape from seemingly formless fertilized eggs. Indeed, for the first experimental embryologists, the most obvious place to look for answers to the mysteries of heredity was not deep in the genome--an entity whose existence they barely suspected--but within the environment of the embryo. During the latter half of the nineteenth century, biologists showed, for example, how different color morphs of the same butterfly species resulted from changes in temperature. Others examined the effects of ion or nutrient levels on development or looked at how environmental factors such as temperature could determine sex.

Then, in the early twentieth century, a confluence of discoveries and new technologies turned the attention of most biologists to genetics and physiology. Increasingly, in the West, biologists saw every individual as a self-contained unit whose study could answer virtually every biological question. Developmental biologists focused their attention on laboratory experiments in which the role of the environment was deliberately eliminated.

In the Soviet Union, however, biologist Trofim Lysenko believed that environment determined phenotype--that is, all of an organism's observable attributes, both structural and functional. As a student, Lysenko had been laughed at by geneticists; once he rose to power, he denounced old acquaintances and even mentors. Under Stalin and Lysenko, an entire generation of Soviet geneticists was exiled or murdered. Those who survived fled to Europe or to North or South America.

Biologists in the West recoiled violently from Lysenkoism. Many had lost personal friends in the purge or were themselves expatriate Soviets who had fled. The very idea that the environment influences phenotype became associated with the worst aspects of Stalin's bloodthirsty reign, with Communism, and with left-wing politics in general--but not with science.

In the 1940s and 1950s, a handful of Europeans and Americans attempted to reintroduce environmental considerations into developmental biology but met with little success. The molecular genetics revolution of the 1960s swept up many of the brightest young minds. Throughout the 1960s and 1970s, biologists interested in the effects of environment on development, survival, and reproduction worked primarily in ecology, agriculture, conservation biology, and related fields.

As developmental biologists increasingly focused on how genes "determine" phenotype, they turned to just a handful of "model" organisms that would reproduce rapidly and easily, primarily in the laboratory. Studies of the development of six animals--nematode worms, Drosophila fruit flies, zebra fish, African clawed frogs, domestic chickens, and house mice--formed the basis for nearly all we know about the genetics of development in animals. All six share certain traits, such as rapid development and early sexual maturation, that tend to minimize the effects of environment.

Jessica Bolker, an evolutionary developmental biologist at the University of New Hampshire, has argued that biologists, in choosing organisms little affected by the environment, have unwittingly reinforced assumptions about the primacy of genes. All six of these lab organisms give molecular genetics the answer it expects, namely, that genes rigidly program development, independent of the environment of the embryo. As Bolker says, "Most of our models are small and fast and hardwired.... And so we think of development as being hardwired."