CARSON, HAMPTON LAWRENCE

(b. Philadelphia, Pennsylvania, 5 November 1914;

d. Honolulu, Hawaii, 19 December 2004), cytogenetics, evolutionary theory.

Carson was one of the pioneers in applying cytogenetic analysis of chromosome structure, particularly inversion patterns, to tracing evolutionary migrations, population divergences, and speciation. He was a member of the National Academy of Sciences, the American Academy of Arts and Sciences, the Society for the Study of Evolution (president, 1971), American Society of Naturalists (president, 1973), the Genetics Society of America (president, 1981), and the American Association for the Advancement of Science. He was a Fulbright research scholar at the University of Melbourne (1961) and served as a visiting professor of biology at the University of São Paulo, Brazil (1961, 1977). He was also a member of the Wheelock Expedition to Labrador (1934). To Carson, one of his greatest honors was receiving the Joseph Leidy Medal from the Academy of Natural Sciences in Philadelphia (1985).

Background and Education . Carson came from an old Philadelphia family with a strong professional background (his great-grandfather, Dr. Joseph Carson, was a botanist and professor of materia medica at the University of Pennsylvania and his father a prominent lawyer). He credited his initial interest in natural history to examining insects and other organisms under his great-grandfather’s small antique microscope. Carson graduated with a major in zoology (1936) and subsequently pursued his PhD (1936–1943) at the University of Pennsylvania. His interest shifted from birds to insects as models for investigating mechanisms of evolutionary change. Carson spent the rest of his career working on the cytogenetics and geographic distribution of several insect species, mostly the fruit fly Drosophila. He remained an avid field biologist all his life, going on one of his last field trips in 2004, at the age of ninety.

His full-time teaching positions included twenty-seven years at Washington University in St. Louis, where he served as assistant, associate, and full professor (1943–1970), and as professor of cell and molecular biology at the University of Hawaii, where he remained for the rest of his career (he became emeritus in 1985). Carson was active in publishing (his last papers were on mate-choice in Drosophila in 2002, 2003) and presenting seminars (his final one was a Sesquicentennial Lecture in the Biology Department at Washington University in April 2004). He died from metastasized bladder cancer in December 2004.

Carson entered the University of Pennsylvania as a freshman in 1932, intending to become a lawyer. Harboring an interest in natural history, he soon took up bird-watching seriously. He studied under Clarence E. McClung, a cytologist of note who had been among the first to suggest that the accessory chromosome (later known as the “X” chromosome) was associated with sex determination. Under McClung, a meticulous investigator with little taste for large-scale theorizing, Carson first studied development of the apical cell in spermatogenesis in insects. The apical cell is close to the sperematogonia, the cells that actually give rise to sperm, and McClung, who believed in the inheritance of acquired characteristics, thought that influences from the environment could be transferred to the spermatagonia via the apical cell. After two years, Carson had not found much, and the aloof McClung retired in 1934.

Carson then studied under Charles W. Metz, a student from Thomas Hunt Morgan’s laboratory at Columbia (PhD, 1916), who was McClung’s successor as head of the laboratory. Metz specialized in the genetics of diptera, including Drosophila and Sciara. Unlike McClung, Metz took more direct interest in his students, and in particular fostered Carson’s growing interest in genetics and its relationship to evolution. That interest was given considerable boost from two books: Cyril D. Darlington’s Recent Advances in Cytology(1932) and Theodosius Dobzhansky’s Genetics and the Origin of Species (1937). Darlington’s book spoke directly to Carson’s interest in the relationship between cytology and evolution. Unlike many cytologists of his day, Darlington was willing to theorize and speculate about cell structures and functions in a free and uninhibited way. In particular, he emphasized the importance of understanding the cytological structure of chromosomes as bearing on the nature of variation and selection. Darlington pointed out that variations in chromosome structure (inversions, deletions, transpositions, and duplications) could be as important as point mutations as a source of variation on which selection could act. He thus stressed the importance of cytological investigation of those structural rearrangements and their effects on phenotypic variation. However, senior biologists viewed Darlington’s book with suspicion and outright hostility. Carson reported that he had to keep his copy of Recent Advances inside his desk drawer because most of the faculty thought it was “dangerous” material for graduate students to read.

In contrast, Dobzhansky’s book, based on his Jessup Lectures at Columbia, was far more acceptable to the genetics establishment. Dobzhansky suggested a variety of ways in which genetics, including chromosomal rearrangements, could provide the foundation for understanding the mechanism of variation and thus of evolution. In particular, Dobzhansky was just beginning his use of chromosome morphology to distinguish between genetically heterogeneous populations of Drosophila in the wild. For Carson, the synthesis of genetics and evolution through cytology was greatly reinforced when, in 1939, Dobzhansky visited the Penn labs to give a seminar. As Carson recalled, Dobzhansky

walked into my lab and I had an inversion configuration from Sciara under the microscope, which I thought was a transposition. In other words, a section of bands was not in the right place. It was moved down the chromosome, but the rest of the chromosome was in the expected order, and he said, “Oh, Carson, that is two inversions, but they’re overlapping one another.” He made a diagram to show how that worked. (quoted in Anderson, Kaneshiro, and Giddings, 1989, p. 6)

Through Dobzhansky, Carson was also introduced to the Russian school of population genetics, particularly the work of Nikolai I. Dubinin, which among other things made clear the importance of combining field and laboratory work.

At Metz’s suggestion, Carson undertook for his thesis a study of the geographic distribution of inversions in polytene chromosomes (chromosomes that have replicated many times without the daughter strands separating, thus producing a much-enlarged, and more visible structure under the microscope) of Sciara. Among the various consequences of inversions, crossing-over, or exchange of genetic information between two homologous chromosomes is greatly reduced or prevented in the inverted region. What this meant from an evolutionary perspective was that blocks of advantageous genes, especially ones that functioned together adaptively (epistatically), would be preserved as a group. Thus inversions could be seen as an important evolutionary mechanism for preserving adaptive groups of genes. Carson proceeded to survey a number of populations of Sciara in the eastern United States, noting that different populations could be characterized by the frequency of particular inversions. Although Carson did not yet have an explicitly evolutionary focus for his research, the idea of using a detailed cytological record of inversions as a means of exploring evolutionary relationships was already beginning to emerge in his thinking.

As Carson was finishing his dissertation in November 1942, Viktor Hamburger, chair of the Zoology Department at Washington University in St. Louis, offered him a position as assistant professor. In January 1943, Carson drove to St. Louis to take up his new position. His wife Meredith and young son Eddie, were to follow shortly by train. Carson’s first teaching assignment was two advanced lecture/laboratory courses, one in parasitology and the other in protozoology. His only preparation was having taken a course in each subject while at Penn, and his only resources were the course and lab outlines and slides left by his predecessor.

From Sciara to Drosophila . Carson found the intellectual atmosphere in the Zoology Department at Washington University congenial and stimulating. Hamburger encouraged faculty members and graduate students to organize informal gatherings and journal clubs, to which he would often invite his former European colleagues when they visited St. Louis. Carson recalls meeting the embryologists Johannes Holtfreter and Salome Gluecksohn-Waelsch, and the geneticist Curt Stern, as well as local faculty such as the biochemists Carl and Gerti Cori (future Nobel laureates for their work on the initial stages of carbohydrate metabolism) and the neurophysiologist George Bishop (a specialist in the physiology of the central nervous system), all of whom took interest in his work.

Of more immediate and practical importance was his association with two colleagues, the plant geneticist Edgar Anderson, Engelmann Professor in the Henry Shaw School of Botany (counterpart to the Zoology Department and housed in the same building), and another recent arrival in the Zoology Department, Harrison D. “Harry” Stalker, a student of Curt Stern’s at Rochester. Anderson was a superb field naturalist as well as a well-trained geneticist (he was a student of Edward M. East at Harvard’s Bussey Institution). He was also, like Carson, interested in the relationship between genetics and evolution, and was to propose, in 1949, the influential theory of introgressive hybridization as a mechanism of evolution in plants. Carson attended Genetics and Natural History, a course developed by Anderson in which students went on field trips and were told simply to observe “the sunflower” in the field and find something interesting to study about its genetics. Carson found numerous polytene chromosomes inside the sunflower heads, which he playfully claimed at first to belong to sunflower seeds. He later told Anderson and the class that they were actually from the salivary glands of the larvae of a very small fly that lived in the sunflower seed. The mixture of genetics and field work appealed to Carson’s naturalist background.

Carson’s association with Stalker proved to be more serious and long-lasting. Stalker was interested in the morphometrics of Drosophila and had written to Alfred H. Sturtevant at the California Institute of Technology, who had worked out the first chromosome map in Drosophila melanogaster in 1911. Stalker had asked Sturtevant what species of Drosophila needed to be worked on, and Sturtevant had suggested D. robusta, because it had numerous inversions that affected size, growth rates, and other morphometric characteristics. Stalker had no familiarity with cytology, and because Carson had worked on inversions in Sciara, Stalker suggested they collaborate: he would do the morphometrics and Carson could work out the inversions. Sturtevant generously sent them a manuscript of a paper in which he had outlined some of the inversions he had observed in robusta, telling the young investigators they could do with the findings anything they wanted, as he was not going to publish it. Carson’s collaboration with Stalker produced a series of papers over the decade 1945– 1955, using inversions—the type, frequency, and changes over time—to determine the structure and evolution of natural populations. For example, they noted correlations between specific inversion figures, inherited phenotypic characters (determined by controlled laboratory breeding experiments), and geographic distribution (north-south or altitudinal gradients). This work followed directly in the vein of Dobzhansky’s study of Drosophila pseudo-obscura populations across the southwest. Such studies suggested that certain gene arrangements were more adaptive under one set of environmental conditions (seasonal, or climatic) than others. Such changes opened the door to investigation in the laboratory of exactly how certain gene complexes could be selected for or against by environmental factors. On the genetic side these findings also supported laboratory work, showing that the final phenotypic form of most traits are the result of interaction between environmental factors and multigene complexes.

Carson and Stalker worked together in complementary ways. Stalker had a down-to-earth view of science that emphasized data collection, and shied away from large-scale theorizing. He was a careful and thorough quantitative biologist who firmly believed that if enough data were available theoretical conclusions would follow logically. He was skeptical of generalizations, and as Carson reported, he “always had a dozen reasons why an idea or research plan or theoretical notion was no good” (Anderson, Kaneshiro, and Giddings, 1989, p. 10). Carson was interested in theoretical issues, in using organisms and their chromosomes to answer larger questions about the evolutionary process, particularly the mechanism of speciation. Gradually, Carson began to work on other projects, though he and Stalker remained close friends throughout their careers.

The Hawaiian Drosophila Project . In 1962 Carson had a conversation with Wilson Stone from the University of Texas about a project Stone and Elmo Hardy from the University of Hawaii were organizing to study the distribution and genetic makeup of the various species of Drosophila in the Hawaiian archipelago. In 1963 Stone invited Carson (and Stalker) to take part in a grant he was preparing with Marshall Wheeler for National Science Foundation (NSF) funding. Carson and Stalker agreed, and the Hawaiian project was to become the focus of their work, particularly Carson's, for the rest of his career (Stalker eventually bowed out, especially after Carson

moved to Hawaii). Initially Stone’s and Hardy’s aim was to develop methods of collecting and rearing the various species in the laboratory, because none of the methods used with North American species seemed to work with the Hawaiian groups (they were more fragile and easily damaged by collecting with nets; the larvae did not eat the usual banana-fruit food and would not pupate in the culture vials). A good part of the group’s initial work was directed to solving these problems.

Once a multitude of technical problems were resolved, it became clear that the Hawaiian Drosophila offered an incredibly rich field and laboratory system with which to study evolution. Carson began to find all sorts of new inversion patterns. Comparing them to each other and with the mainland North American species, he and Stalker made several important and novel observations. Of the 250 species found within the archipelago all but about twelve were endemic, meaning they had evolved in the Hawaiian archipelago and were found nowhere else. The Hawaiian group comprised about one-fourth of all the Drosophila species in the world known at that time. Because the oldest of the Hawaiian islands (Kauai, the northwest end of the archipelago) is only 5.6 million years old, and the youngest (Hawaii, at the southeastern end) is only about 700,000 years old, evolutionary radiation has been extensive and rapid. Hybridization studies, carried out largely by the Texas colleagues of the project, showed that no fertile hybrids were produced from crosses between any of the Hawaiian species.

Carson was able to use his examination of inversions in a large number of species to propose a pattern of migration between the islands that proceeded from the oldest (Kauai) to the youngest (Hawaii) island. The basic method was simple: Carson compared inversions in different species to each other and to a standard chromosome arrangement from Drosophila grimshawi, chosen as the likely progenitor of the others. For practical purposes Carson concentrated on a large subset of species called the “Picture-Wing” Group, a name derived from the characteristic markings on their wings, noting differences in inversion patterns of their chromosomes. The more similar the pattern, he reasoned, the more recently two species diverged. As might be expected, the patterns differed most widely between species on the two most distant islands, Kauai and Hawaii, with intermediates in the intervening islands. However, backward migrations also seemed to have occurred, as suggested by the arrows labeled 1 and 7 in Figure 1. These studies, in the 1960s, led Carson to consider the relationship between migration events by “founder” organisms and the formation of new species.

Founder-Flush and Speciation . The Hawaiian Drosophila system allowed Carson to address several important theoretical questions about the process of speciation that had been of interest to him and had been widely debated among evolutionary biologists ever since Darwin. By the mid-twentieth century most investigators more or less agreed on several points: divergent speciation required the migration of some “founder” individuals out of the parent species’ range to a new locale. The founder group most likely to lead to the formation of a new and successful divergent line would be one that harbored considerable genetic diversity, allowing it to adapt more readily to new conditions. It was also held that the founder population would have to remain geographically isolated from the parent population for a long enough period that genetic variations could accumulate to a sufficient degree that the two populations could no longer interbreed (what is called allopatric speciation). Finally, it was clear to many evolutionists that the basic mechanism of microevolution—selection acting on slight individual genetic differences—was not likely by itself to lead to speciations. Some other processes and conditions were necessary, but what those conditions were and how speciation actually took place were not well worked out. Carson’s “founder-flush” model was one attempt to provide a new model.

Based in part on some of the work of Ernst Mayr, and his own studies of the Hawaiian Drosophila, Carson’s model suggested that migration of a few, or even one (such as a gravid female) organism could be enough to initiate a founder event. His own studies on inversions showed that there was considerable genetic variation (individuals heterozygous for one or more inversions) in natural populations (there was debate as to whether there was more variation at the center or periphery of a population’s range). Along with Mayr, Carson thought genetic divergence of the founder population would be enhanced not only by heterozygosity but also by the random sampling error introduced by migration of just a few organisms from the original population. In the new environment, freed from the constraints imposed by rigorous competition and selection in the large, dense, parent population), the variability in the founder population might confer a greater chance of survival. Borrowing Mayr’s concept of a “genetic revolution” in a founder population, Carson saw inversions, in particular, as serving two very different roles that would both foster and preserve new variability. On the one hand, because the genome functions as an integrated whole, new combinations of inversions could lead to new phenotypes that might prove adaptive to the new environment. On the other hand, inversions preserved successful combinations of genes and thus helped to stabilize the founder population’s genetic makeup.

Under these conditions a founder population could undergo rapid expansion, producing what Carson called a “flush” period. During the flush period Carson saw the process that actually transformed the old species into a new one by means of Sewall Wright’s shifting-balance concept, in which the population shifted from its old to a new genetic constitution and to a new adaptive landscape. The flush period led eventually to high density and “over-population,” followed by a “crash” period, in which the population would shrink considerably in size. In each crash period random sampling error could again produce a significant change in the population’s genetic composition that could (but not necessarily would) lead to further divergence. The Hawaiian Drosophilas, in their multiple migrations among the islands provided the perfect example of how a founder-flush model for speciation could occur. Carson first put forth his “founder-flush” model at the 1955 Cold Spring Harbor Symposium on Quantitative Biology.

Following Dobzhansky, Carson tested his founder-flush model with laboratory experiments, using population chambers where environmental conditions could be controlled, and into which he could introduce flies in all sorts of combinations (a single gravid female, or flies with known inversions) and observe changes in genotypes/phenotypes over a specified number of generations. For example, in one experiment he placed into an inbred population of flies with recessive mutant markers one male fly whose mother was from the population but whose father was from a wild-type laboratory strain. Keeping food, space, and all other conditions constant, he noted that a population flush ensued so that within nine generations the population size had tripled. He reasoned that introducing the wild-type genes had produced, through hybridization, a new gene pool with higher Darwinian fitness in at least some of the genotypes produced by mixing the wild-type with the inbred mutant strain. Thus a population flush could be induced by introducing novel genetic elements, as well as by other more conventional causes such as decreased predation or increased food supply.

Carson’s work was highly influential, stimulating a whole generation of evolutionary biologists to investigate the process of speciation from a population genetic perspective. As the historian William Provine has remarked, Carson's

theorizing has always been very closely tied to experimental evidence. He began thinking about founder effects and genetic revolutions at a time when direct evidence from natural populations was almost entirely absent. My conclusion is that the evidence from natural populations and from laboratory experiments concerning founder effects and genetic revolutions grew and changed dramatically between 1955 and 1975, in large part from Carson’s own researches and those stimulated by him. (Provine, 1989, p. 69)

Among those who owe a considerable debt to Carson are Alan Templeton (his undergraduate student at Washington University), Brian Charlesworth, Nicholas H. Barton, and William L. Brown, even when those individuals sometimes disagreed strongly with his ideas.

Assessment . Carson’s work systematically brought together the ideas of a number of evolutionary thinkers, both from the past and from among his contemporaries. Four of particular importance were represented by portraits on the wall of his office at the University of Hawaii: Charles Metz, John T. Gulick (who grew up in Hawaii and after reading Darwin recognized the importance of the Hawaiian biota for evolutionary theory), Theodosius Dobzhansky, and Sewall Wright. (A fifth portrait was of Viktor Hamburger, who gave Carson’s career such a promising start.) Others from whom he drew inspiration included Cyril D. Darlington (for uniting cytogenetics and evolutionary theory) and Ernst Mayr (for his synthetic views on species and speciation). Carson thought of himself as a synthesizer, bringing together not only genetics, cytology, and evolutionary theory, but also the combined field and laboratory approaches so necessary to understanding evolution of real populations in nature. As he wrote in 1980, his work in cytogenetics and evolution “shows how advancing understanding tends to unify knowledge by the removal of the artificial walls that man erects as he fumbles along. At this juncture we would do well to sharpen our perception to identify barriers [to our thinking] as yet only dimly seen” (Carson, 1980, p. 92).

BIBLIOGRAPHY

A complete bibliography of Carson’s publications from 1934 to 1989 can be found in Genetics, Speciation, and the Founder Principle,edited by Luther Val Giddings, Kenneth Y. Kaneshiro, and Wyatt W. Anderson, pp. 28–41. New York: Oxford University Press, 1989.

WORKS BY CARSON

With Harrison D. Stalker. “Gene Arrangements in Natural Populations of Drosophila robusta Sturtevant.” Evolution 1 (1947): 113–133.

“The Genetic Characteristics of Marginal Populations of Drosophila.” Cold Spring Harbor Symposium on Quantitative Biology 20 (1955): 276–286.

“The Species as a Field for Gene Recombination.” In The Species Problem, edited by Ernst Mayr, 23–38. Science Publication no. 50. Washington, DC: American Association for the Advancement of Science, 1957.

“Response to Selection under Different Conditions of Recombination in Drosophila.” Cold Spring Harbor Symposium on Quantitative Biology 23 (1958a): 291–306.

“Increase in Fitness in Experimental Populations Resulting from Heterosis.” In Proceedings of the National Academy of Sciences of the United States of America44 (1958b): 1136–1141.

“Genetic Conditions Which Promote or Retard the Formation of Species.” Cold Spring Harbor Symposium on Quantitative Biology 24 (1959): 87–105.

“The Population Flush and Its Genetic Consequences.” In Population Biology and Evolution: Proceedings of the International Symposium, June 7–9, 1967, Syracuse, New York, edited by Richard C. Lewontin, 123–137. Syracuse, NY: Syracuse University Press, 1968.

“Chromosome Tracers of the Origin of Species.” Science 168 (1970): 1414–1418.

“The Genetics of Speciation at the Diploid Level.” American Naturalist 109 (January–February 1975): 83–92.

“Cytogenetics and the Neo-Darwinian Synthesis.” In The Evolutionary Synthesis: Perspectives on the Unification of Biology, edited by Ernst Mayr and William Provine, 86–95. Cambridge, MA: Harvard University Press, 1980.

With Alan R. Templeton. “Genetic Revolutions in Relation to Speciation Phenomena: The Founding of New Populations.”

Annual Reviews of Ecology and Systematics 18 (1984): 97–131.

“Inversions in Hawaiian Drosophila.” In Drosophila Inversion Polymorphism, edited by Costas B. Krimbas and Jeffrey R. Powell, 407–453. Boca Raton, FL: CRC, 1992.

“A New Era in Science at Washington University, St. Louis: Viktor Hamburger’s Zoology Department in the 1940s.” International Journal of Developmental Neuroscience 19 (2001): 125–131.

“Mate Choice Theory and the Mode of Selection in Sexual Populations.” In Proceedings of the National Academy of Sciences of the United States of America 100 (2003): 6584–6587.

OTHER SOURCES

Anderson, Wyatt, Kenneth Y. Kaneshiro, and Luther Val Giddings. “Hampton Lawrence Carson: Interviews toward an Intellectual History; List of Publications from 1934 to 1989.” In Genetics, Speciation, and the Founder Principle, edited by Luther Val Giddings, Kenneth Y. Kaneshiro, and Wyatt W. Anderson, 3–41. New York: Oxford University Press, 1989. The interviews provide useful insight into the various influences that stimulated Carson from his student days onward.

Dobzhansky, Theodosius. “Adaptive Changes Induced by Natural Selection in Wild Populations of Drosophila.” Evolution 1 (1947): 1–16.

Provine, William B. “Founder Effects and Genetic Revolutions in Microevolution and Speciation: An Historical Perspective.” In Genetics, Speciation, and the Founder Principle, edited by Luther Val Giddings, Kenneth Y. Kaneshiro, and Wyatt W. Anderson, 43–76. New York: Oxford University Press, 1989. Has a section on Carson’s work but the article as a whole traces the much wider discussion of founder effects.

Garland E. Allen