Two foundational developments of modern biology—the theories of evolution by natural selection and the genetic basis of heredity—were built from the language, arguments, evidence, and practices of controlled breeding in agriculture and the laboratory. The genotype-phenotype distinction—or, rather, a series of different meanings of those terms—provides an entry point into the implications of that genesis and subsequent developments. Complexities get suppressed, which engenders new problems and complexity-recovering responses. Many of these are raised or implied by Johannsen (1911), where the terms genotype and phenotype were introduced to English-language readers.
1. Establish repeatable outcomes and expose hidden processes. The overarching problem for Johannsen was to promote a shift from “morphological-descriptive” natural history, in which appearances could mislead and obscure, or be spun into speculative theories, to an “exact science,” using the experimental control of biological materials and conditions needed to establish repeatable outcomes and expose hidden processes. This problem can be positioned in relation to the cultural history of heredity in Europe (Müller-Wille, Rheinberger and Dupré 2008) in general and to Johannsen’s professional and modernizing aspirations in particular (Müller-Wille 2008). However, for our purposes, only the conceptual and methodological dimensions of Johannsen’s work will be considered. Problem 1 will be returned to after introducing six other problems.
2. Alternative to transmission-conception of heredity. A specific conceptual-methodological variant of problem 1 was to articulate an alternative to traditional accounts of heredity that, in Johannsen’s words, “triedto conceive or ‘explain’ the presumed transmission of general or peculiar characters and qualities ‘inherited’ from parents or more remote ancestors.” In rejecting a “transmission-conception” of heredity, he sought specifically to depart from a) the biometricians’ analysis of continuous variation, which showed traits of offspring to be numerically correlated with those of their parents, grandparents, and so on, and thus preserved the possibility of ancestral influences; and b) particulatetheories, such as those of Weismann and Darwinians that could be seen as consistent with transmission of parental traits to the zygote (the initial cell resulting from a fusion of egg and sperm), because the “elements responsible for inheritance [were held to] involve the different organs or tissue-groups of the individual developing from the zygote.”
Johannsen’s alternative involved four initial steps: i) accepting the part of Weismann’s theory of the germplasm in which certain cells are sequestered early in the development of an organism, buffered from most of the interactions within the organism and with the environment that occur during the organism’s lifetime, and form a basis for development of an organism of the next generation; ii) acknowledging that “the objects for scientific research” are the “’types’ of organisms distinguishable by direct inspection or… by finer methods of measuring or description, [which] may be characterized as ‘phenotypes.’ Certainly phenotypes are real things”; iii) hypothesizing distinguishable classes of organisms that share germplasm, classes that he called genotypes; and iv) demonstrating i-iii. above using experimentally generated phenotypes, namely, inbred lines of beans.
In these experiments, the plants in any line showed variation yet selection for some desired trait had not resulted in improvement from one generation to the next. Whatever the germplasm was that seeds from a line shared and in whatever ways it “reacted” during the plant’s development, “interfering with the totality of all incident factors, may it be external or internal,” seeds of the next generation did not result in plants that matched their parent any more than from any other seed. Plants from the inbred line were instances of a genotype; variation in the traits grown from the seeds was, borrowing from Wolterek, the norm of reaction (Reaktionsnorm) of that genotype; a plant’s relative position in the norm of reaction was not transmitted to its offspring; and (with the emphasis Johannsen’s) “selection is not able to shift the nature of genotypes.” In short, the genotype conception of heredity was “ahistoric.”
3. Unambiguous use of phenotypes to distinguish genotypes. Even in the realm of inbred lines, phenotypes might, Johannsen noted, be heterogeneous—a mix of several genotypes (as illustrated by the sole figure in Johannsen 1911). To remove the ambiguity of appearance—to be able to use phenotypes to distinguish genotypes—he relied on research that was flourishing after the rediscovery of Mendel’s experiments on peas. Those experiments can be summarized as follows:
In summary, although the F1 hybrids appeared the same as one of the inbred parents, the hybrids could, through the ratios of the two traits in the F2 generation, be shown to belong to a different, in Johannsen’s terms, genotype—a heterozygote, not a homozygote. Against the traditional “transmission-conception” of heredity, the reappearance in F2 of traits not visible in F1 could be explained without any “ancestral influence.” The dichotomous nature of Mendel’s traits was in line with Johannsen wanting to distance his views from the analysts of continuous variation (a. in problem 2). On the other hand, trait-specific factors—for which he coined the term gene—did not help distance his conception from particulate theorists (b. in problem 2).
4. Once genotypes are distinguishable, meanings of terms can shift. If the inbreeding, crossing, and self-pollination used in Mendelian research were to be seen as “finer methods of measuring or description,” then the inbred parent would be classified as a different phenotype from the F1 hybrid. If so, the study of heredity Johannsen seeks would be to find or generate phenotypes—classes of organisms distinguished by traits—that are isomorphic with genotypes—classes of organisms defined by shares germplasm. Yet what counted as a phenotype had become a secondary matter; what was important to Johannsen was to have a means to distinguish genotypes. Even if “differences between the phenotype-curves [that result from reactions of different genotypes under various conditions] may vary considerably or may even vanish entirely,” a specific “genotypical constitution always reacts in the same manner under identical conditions.”
Having established that genotypic stability, it made sense to shift the focus in studies of heredity from the primacy of genotypes to the germplasm shared by a genotype. This is what Johannsen began to do in referring to the genotypical constitution. Indeed, his article prefigured a shift that soon became the norm wherein genotype came to refer not to a class of organisms but to specific constituents of the germplasm: “A ‘genotype’ is the sum total of all the ‘genes’ in a gamete or in a zygote.” The original use of phenotype to denote a discernable class of organisms, to be mapped to genotype as a class of organisms, could, in turn, be put aside (and, indeed, is now archaic). When Johannsen wrote “phenotypes… i.e., the reactions of the genotypical constituents,” he prefigured the use of the term to refer to the set of an organism’s traits associated with a genotype under given conditions. That shift of meaning, it should be noted, reverses the direction of mapping.
5. Continuous variation; discontinuous genotypes (extending a. under problem 2). Just as a distinct phenotype might be a mix of several genotypes, continuous variation in regular populations (i.e., not inbred lines) did not contradict the discontinuity of genotypes: “The well-known displacement… of a population… proceeding from generation to generation in the direction indicated by the selection—is due to the existence a priori of genotypical differences in such populations.” Such selection changed the relative proportion of genotypes in the population, not any genotype itself. This avenue of potential reconciliation with the biometrical view of variation in non-experimental populations was not, however, pursued by Johannsen (see problem qq). Instead, like other Mendelians of that time, he chose to dispute the idea that different types of organism could be “evolved from each other by extremely small steps in genotypical change”: “the mutations really observed in nature have all shown themselves as considerable, discontinuous saltations.”
6. The germplasm as a whole; particulate genes (extending b. under problem 2). Mendelian experiments countered the “transmission-conception” by affirming Weismann’s theory of a germplasm unchanged by reaction to conditions during development in the previous generation. At the same time, the experiments promoted a particulate view of heredity in that two factors or genes influenced a given trait. Johannsen wanted to maintain an emphasis on the genotype as a whole: “[C]haracters may be determined by several different genes, and… one sort of gene may have influence upon several different reactions.” “[T]he talk of ‘genes for any particular character’ ought to be omitted…” To turn this view into “exact science,” some method for analyzing the genotypical constitution or genotype as a whole was needed. He did not, however, provide one.
Mendel’s experiments exacerbated the problem: the traits of the peas were not only dichotomous, but independently assorted—there was no pattern of co-occurrence of variants of the different traits, as would be the case, say, if crinkly peas occurred more often on dwarf plants. It made sense to talk of a pair of factors or genes for crinkly peas. Admittedly, the new Mendelian research showed that independent assortment to be a special case, yet the particulate view remained central to experiments involving crosses between lines that, as much as possible, were inbred and, other than for the traits under study, were identical and homozygous for genes influencing all traits. The identical homozygous genes may still have an influence on the focal trait, but differences in that trait could be attributed to differences in the non-identical genes in the crossed lines.
To the extent that Mendelian methods could expose the influences of specific pairs of genes (or a small set of pairs of genes), the genotype could be redefined further so it referred to a specified part of the germplasm (or, adapting the original meaning of genotype, to the class of organisms sharing that part of the germplasm). The corresponding phenotype could be defined in terms of the subset of the organism’s traits associated under given conditions with that redefined partial genotype (or to the class of such organisms). The remaining germplasm, moved into the background, might be identical in inbred lines, but, in general, could vary among the individuals in a population.
7. The organism as a whole; particulate genes. Johannsen raised another problem about particulate genes when he asserted that the traits “of the organism in toto are the results of the reactions of the genotypical constitution” (his emphasis) and found no “suggestive value” in the idea that “discrete particles of the chromosomesare ‘bearers’ of special parts of the whole inheritance in question.” He noted that “there may be… very narrow limits for [Mendelian] analysis: the entire organization may never be ‘segregated’ into genes.” To put this another way, the influence of genotypic constituents that are identical for all members of a species cannot be studied through Mendelian crosses. The “genotype-conception” of heredity, by centering on genotypic differences associated with phenotypic differences, shifted attention away from the species-typical germplasm. Mendelian analysis focused on dissimilarity over similarity, even though both aspects were included in prevailing conceptions of heredity (Sapp 1983)—for the eye color of a group of fruit flies to differ from the rest of the population, there have to be fly zygotes able to develop into organisms that have eyes with color.
This last point returns us to problem 1 in that the morphological side is downplayed by the pursuit of experimentally generated and repeatable outcomes. However, the descriptive side persists in Johannsen’s original definitions of phenotype and genotype as classes of organisms and even in his discussion of genotypic constituents. Their material make-up and development—the processes through which the germplasm reacts or “interfere[es] with the totality of all incident factors”—lie outside the scope of Johannsen’s genotype-conception of heredity: “[T]he nature of the “genes”… is as yet of no value to propose any hypothesis.” The Mendelian researchers who adopted and adapted Johannsen’s new terms—gene, genotype, phenotype—were not so conservative…. (to be continued–or revised)