J Appl Genet 50(3), 2009, pp. 177–184 Review article Darwin’s contributions to genetics Y-S. Liu1,2, X-M. Zhou1, M-X. Zhi1, X-J. Li1, Q-L. Wang1 1Henan Institute of Science and Technology, Xinxiang, China 2Department of Biochemistry, University of Alberta, Edmonton, AB, Canada Abstract. Darwin’s contributions to evolutionary biology are well known, but his contributions to genetics are much less known. His main contribution was the collection of a tremendous amount of genetic data, and an at- tempt to provide a theoretical framework for its interpretation. Darwin clearly described almost all genetic phe- nomena of fundamental importance, such as prepotency (Mendelian inheritance), bud variation (mutation), heterosis, reversion (atavism), graft hybridization (Michurinian inheritance), sex-limited inheritance, the direct action of the male element on the female (xenia and telegony), the effect of use and disuse, the inheritance of ac- quired characters (Lamarckian inheritance), and many other observations pertaining to variation, heredity and development. To explain all these observations, Darwin formulated a developmental theory of heredity – Pan- genesis – which not only greatly influenced many subsequent theories, but also is supported by recent evidence. Keywords: Darwin, genetics, Pangenesis, variation and heredity, breeding. Introduction and so forth.” Darwin’s interest in genetics was a consequence of his studies of evolution. He fully In 1906, the late William Bateson coined the word realized that his theory of natural selection must be genetics in his inaugural address to the Third Con- based on a sound understanding of the mechanism ference on Hybridization and Plant-Breeding: “I of inheritance. One of the striking things about suggest for the consideration of this Congress the Darwin was that he had a detailed firsthand knowl- term Genetics, which sufficiently indicates that edge of both animals and plants, and painstakingly our labours are devoted to the elucidation of the collated every bit of information about heredity phenomena of heredity and variation: in other that he found in the literature (Sturtevant 1965). words, to the physiology of Descent, with implied Darwin saw and clearly described almost all ge- bearing on the theoretical problems of the evolu- netic phenomena of fundamental importance and tionist and the systematist, and application to the formulated a developmental theory of heredity – practical problems of breeders, whether of animals Pangenesis. Thus in Bateson’s opinion, Darwin or plants” (Bateson 1906). was a pioneer of genetics, because “Darwin made More than 100 years after the introduction of a more significant contribution. Not for a few gen- the science of genetics, Darwin’s contributions to erations, but through all ages he should be remem- genetics are still not well known. As early as in bered as the first who showed clearly that the 1859, Darwin predicted the emergence of the sci- problems of heredity and variation are soluble by ence of genetics. In the last chapter of The Origin, observation, and laid down the course by which we read: “A grand and almost untrodden field of we must proceed to their solution. Evolution is a inquiry will be opened, on the causes and laws of process of variation and heredity. The older writ- variation, on correlation, on the effects of use and ers, though they had some vague idea that it must disuse, on the direct action of external conditions, be so, did not study variation and heredity. Darwin Received: March 3, 2009. Accepted: April 16, 2009. Correspondence: Y. Liu, Department of Biochemistry, University of Alberta, Edmonton, AB, T6G 2H7, Canada; e-mail: [email protected] 178 Y. Liu et al. did, and so begat not a theory, but a science” genes to the offspring, and conversely, if the plant (Bateson 1910). is young, in its first year of bearing, and particu- larly if it is a hybrid of recent origin, its hereditary Darwin’s collection of a tremendous amount of power reaches a minimum” (Michurin 1949). genetic data Yarrell’s law was also confirmed by other re- Prepotency (Mendelian inheritance) searchers (Beardmore et al. 1975; Lizana and Prado 1994). It should be noted that the so-called Many people thought that Darwin did not read Yarrell’s law might be a tendency rather than a Mendel’s paper, thus he did not know Mendelian law, though Darwin believed that “Yarrell’s law inheritance. This is not the case. Segregation in the must be partly true” (Darwin 1987). Mendelian sense was well known to Darwin. In the chapter “Hybridism” in The Origin, Darwin Graft hybridization (Michurinian inheritance) clearly states: “When two species are crossed, one Graft hybridization is a type of asexual hybridiza- has sometimes a prepotent power of impressing its tion, in which heritable changes may be induced likeness on the hybrid; and so I believe it to be by grafting. In 1868, Darwin coined the terms with varieties of plants. With animals, one variety graft hybrid and graft hybridization. In Chapter 11 certainly often has this prepotent power over an- of The Variation, Darwin recorded various cases, other variety” (Darwin 1872). In Chapter 27 of in which shoots that developed from grafted trees The Variation, Darwin wrote: “When two forms have exhibited the characters of both stock and are crossed, one is not rarely found to be prepotent scion, either blended together uniformly or dis- in the transmission of its characters over the other; posed in a mosaic of the parental types. He men- … for instance, there is a latent tendency in all pi- tioned that such shoots are sometimes capable of geons to become blue, and, when a blue pigeon is bearing progenies, which segregate in respect of crossed with one of any other colour, the blue tint their morphological characters and he proposed is generally prepotent”. In the section “Prepotency that they are actually true hybrids. Based on Dar- in the transmission of character” in The Variation, win’s research, Michurin elaborated a simple and Darwin presented an instance of segregation in the efficient method for producing graft hybrids – the second hybrid generation from a cross between mentor-grafting method. Later, graft hybridization peloric and normal-flowered snapdragons: The as a chapter was included in the textbook of first hybrid generation completely resembled the Michurinian genetics. Over the past decades, sev- normal plant, and of the second hybrid generation eral independent groups of scientists have con- of 127 seedlings, 88 proved normal, 37 perfectly firmed the existence of graft hybrids (Frankel peloric, and 2 imperfectly so. This is a good exam- 1956; Ohta 1991; Taller et al. 1999; Stegemann ple of a Mendelian experiment in which there is a and Bock 2009). Recently, grafting experiments single factor difference between the parental proved that endogenous mRNA enters and moves plants, with dominance in the first hybrid genera- the phloem long-distance translocation system tion, and a second generation segregation ratio be- (Lucas et al. 2001). The establishment that novel ing 2.4:1, approaching 3:1. Of course, in Darwin’s mRNA species may move between cells and work it was just one of many examples, not the around the plant, and the ability of retroviruses or crucial mechanism, as it was in Mendel’s research. retrotransposons to reverse transcribe mRNA into Darwin also mentioned Yarrell’s law, which cDNA capable of being integrated into the ge- was named for William Yarrell, a British naturalist nome, indicate that some mechanisms exist for the and animal breeder. Yarrell maintained that a par- horizontal gene transfer from stock to scion and ent of an older breed will have more influence on vice versa by grafting (Liu 2006). the character of the offspring than a parent of a young breed (Darwin 1987). Yarrell’s law was of Bud variation (mutation) great interest to Charles Darwin, as he was trying In his analysis of the causes of biological varia- to understand why certain breeds seemed to have a tion, Darwin encountered several cases in which greater ability to impress their characters on the the characters of the parents were incapable of fu- offspring. Interestingly, Yarrell’s law was later sion and did not show the blending inheritance. He confirmed by Ivan Michurin, who found that old called them sports, spontaneous variations or varieties of fruit plants have a stronger capacity for transmutations. He stated that some few charac- transmitting their characters than young varieties. ters are incapable of fusion but are unimportant, of “The older the plant chosen as a progenitor, the semi-monstrous nature, and have been known to greater is the force with which it transmits its appear suddenly. One of the most striking cases in Darwin’s contributions to genetics 179 animals is that of the japanned or win’s. More recently, Lolle et al. (2005) have black-shouldered peacocks, which have occasion- shown that Arabidopsis plants homozygous for re- ally appeared “suddenly in flocks of the common cessive mutant alleles of the organ fusion gene kind”, but “propagate their kind quite truly”, and (HTH) can inherit allele-specific DNA sequence tend “at all times and in many places to reappear”. information that was not present in the chromo- Concerning useful and ornamental trees, he wrote: somal genome of their parents but was present in “All the recorded varieties, as far as I can find out, previous generations. They proposed a model in have been suddenly produced by one single act of which a type of stable RNA can be replicated and variation”, and as to roses, he remarked on their transmitted over multiple generations. This pro- marked tendency to sport and to produce varieties vides further evidence for reversion or atavism “not only by grafting and budding, but often by (Liu, 2005).