Lamarckism

Lamarckism (or Lamarckian inheritance) is the idea that an organism can pass on characteristics that it has acquired during its lifetime to its offspring (also known as heritability of acquired characteristics or soft inheritance). It is named after the French biologist Jean-Baptiste Lamarck (1744–1829), who incorporated the action of soft inheritance into his evolutionary theories as a supplement to his concept of an inherent progressive tendency driving organisms continuously towards greater complexity, in parallel but separate lineages with no extinction. Lamarck did not originate the idea of soft inheritance, which proposes that individual efforts during the lifetime of the organisms were the main mechanism driving species to adaptation, as they supposedly would acquire adaptive changes and pass them on to offspring.

When Charles Darwin published his theory of evolution by natural selection in On the Origin of Species (1859), he continued to give credence to what he called "use and disuse inheritance," but rejected other aspects of Lamarck's theories. Later, Mendelian genetics supplanted the notion of inheritance of acquired traits, eventually leading to the development of the modern evolutionary synthesis, and the general abandonment of the Lamarckian theory of evolution in biology. Despite this abandonment, interest in Lamarckism has continued as studies in the field of epigenetics have highlighted the possible inheritance of behavioral traits acquired by the previous generation.[1][2][3][4][5] However, this remains controversial as science historians have asserted that it is inaccurate to describe transgenerational epigenetic inheritance as a form of Lamarckism.[6][7][8][9]

History

Jean-Baptiste Lamarck

Between 1794 and 1796 Erasmus Darwin wrote Zoonomia suggesting "that all warm-blooded animals have arisen from one living filament... with the power of acquiring new parts" in response to stimuli, with each round of "improvements" being inherited by successive generations.[10] Subsequently, Jean-Baptiste Lamarck repeated in his Philosophie Zoologique of 1809 the folk wisdom that characteristics which were "needed" were acquired (or diminished) during the lifetime of an organism then passed on to the offspring. He incorporated this mechanism into his thoughts on evolution, seeing it as resulting in the adaptation of life to local environments.

Lamarck founded a school of French Transformationism which included Étienne Geoffroy Saint-Hilaire, and which corresponded with a radical British school of anatomy based in the extramural anatomy schools in Edinburgh, Scotland, which included the surgeon Robert Knox and the comparative anatomist Robert Edmond Grant. In addition, the Regius Professor of Natural History at the University of Edinburgh, Robert Jameson, was the probable author of an anonymous paper in 1826 praising "Mr. Lamarck" for explaining how the higher animals had "evolved" from the "simplest worms"—this was the first use of the word "evolved" in a modern sense. As a young student, Charles Darwin was tutored by Grant, and worked with him on marine creatures.

The Vestiges of the Natural History of Creation, authored by Robert Chambers in St Andrews, Scotland, and published anonymously in England in 1844, proposed a theory which combined radical phrenology with Lamarckism, causing political controversy for its radicalism and unorthodoxy, but exciting popular interest and preparing a huge and prosperous audience for Darwin.

Darwin's On the Origin of Species proposed natural selection as the main mechanism for development of species, but did not rule out a variant of Lamarckism as a supplementary mechanism.[11] Darwin called his Lamarckian hypothesis pangenesis, and explained it in the final chapter of his book The Variation of Animals and Plants under Domestication (1868), after describing numerous examples to demonstrate what he considered to be the inheritance of acquired characteristics. Pangenesis, which he emphasised was a hypothesis, was based on the idea that somatic cells would, in response to environmental stimulation (use and disuse), throw off 'gemmules' or 'pangenes' which travelled around the body (though not necessarily in the bloodstream). These pangenes were microscopic particles that supposedly contained information about the characteristics of their parent cell, and Darwin believed that they eventually accumulated in the germ cells where they could pass on to the next generation the newly acquired characteristics of the parents. Darwin's half-cousin, Francis Galton, carried out experiments on rabbits, with Darwin's cooperation, in which he transfused the blood of one variety of rabbit into another variety in the expectation that its offspring would show some characteristics of the first. They did not, and Galton declared that he had disproved Darwin's hypothesis of pangenesis, but Darwin objected, in a letter to the scientific journal Nature, that he had done nothing of the sort, since he had never mentioned blood in his writings. He pointed out that he regarded pangenesis as occurring in Protozoa and plants, which have no blood.[12]

Lamarck's theory

The long neck of the giraffe is often used as an example in explanations of Lamarckism.

The identification of Lamarckism with the inheritance of acquired characteristics is regarded by some as an artifact of the subsequent history of evolutionary thought, repeated in textbooks without analysis. American paleontologist and historian of science Stephen Jay Gould wrote that in the late 19th century, evolutionists "re-read Lamarck, cast aside the guts of it ... and elevated one aspect of the mechanics—inheritance of acquired characters—to a central focus it never had for Lamarck himself."[13] He argued that "the restriction of 'Lamarckism' to this relatively small and non-distinctive corner of Lamarck's thought must be labelled as more than a misnomer, and truly a discredit to the memory of a man and his much more comprehensive system."[14] Gould advocated defining "Lamarckism" more broadly, in line with Lamarck's overall evolutionary theory.

Lamarck incorporated two ideas into his theory of evolution, in his day considered to be generally true. The first was the idea of use versus disuse; he theorized that individuals lose characteristics they do not require, or use, and develop characteristics that are useful. His second point was to argue that the acquired traits were heritable. Examples of what is traditionally called "Lamarckism" would include the idea that when giraffes stretch their necks to reach leaves high in trees (especially Acacias), they strengthen and gradually lengthen their necks. These giraffes have offspring with slightly longer necks (also known as "soft inheritance"). Similarly, a blacksmith, through his work, strengthens the muscles in his arms, and thus his sons will have similar muscular development when they mature.

Lamarck stated the following two laws:

  1. Première Loi: Dans tout animal qui n' a point dépassé le terme de ses développemens, l' emploi plus fréquent et soutenu d' un organe quelconque, fortifie peu à peu cet organe, le développe, l' agrandit, et lui donne une puissance proportionnée à la durée de cet emploi ; tandis que le défaut constant d' usage de tel organe, l'affoiblit insensiblement, le détériore, diminue progressivement ses facultés, et finit par le faire disparoître.
  2. Deuxième Loi: Tout ce que la nature a fait acquérir ou perdre aux individus par l' influence des circonstances où leur race se trouve depuis long-temps exposée, et, par conséquent, par l' influence de l' emploi prédominant de tel organe, ou par celle d' un défaut constant d' usage de telle partie ; elle le conserve par la génération aux nouveaux individus qui en proviennent, pourvu que les changemens acquis soient communs aux deux sexes, ou à ceux qui ont produit ces nouveaux individus.[15]

English translation:

  1. First Law: In every animal which has not passed the limit of its development, a more frequent and continuous use of any organ gradually strengthens, develops and enlarges that organ, and gives it a power proportional to the length of time it has been so used; while the permanent disuse of any organ imperceptibly weakens and deteriorates it, and progressively diminishes its functional capacity, until it finally disappears.
  2. Second Law: All the acquisitions or losses wrought by nature on individuals, through the influence of the environment in which their race has long been placed, and hence through the influence of the predominant use or permanent disuse of any organ; all these are preserved by reproduction to the new individuals which arise, provided that the acquired modifications are common to both sexes, or at least to the individuals which produce the young.[16]

In essence, a change in the environment brings about change in "needs" (besoins), resulting in change in behavior, bringing change in organ usage and development, bringing change in form over time—and thus the gradual transmutation of the species.

However, as historians of science such as Michael Ghiselin and Stephen Jay Gould have pointed out, none of these views were original to Lamarck.[17][18] On the contrary, Lamarck's contribution was a systematic theoretical framework for understanding evolution. He saw evolution as comprising two processes;

  1. Le pouvoir de la vie (the complexifying force) - in which the natural, alchemical movements of fluids would etch out organs from tissues, leading to ever more complex construction regardless of the organ's use or disuse. This would drive organisms from simple to complex forms.
  2. L'influence des circonstances (the adaptive force) - in which the use and disuse of characters led organisms to become more adapted to their environment. This would take organisms sideways off the path from simple to complex, specialising them for their environment.

Weismann's experiment

August Weismann

The idea that germline cells contain information that passes to each generation unaffected by experience and independent of the somatic (body) cells, came to be referred to as the Weismann barrier, and is frequently quoted as putting a final end to Lamarckism and theory of inheritance of acquired characteristics.

August Weismann conducted the experiment of removing the tails of 68 white mice, repeatedly over five generations, and reporting that no mice were born in consequence without a tail or even with a shorter tail. He stated that "901 young were produced by five generations of artificially mutilated parents, and yet there was not a single example of a rudimentary tail or of any other abnormality in this organ."[19]

However, the experiment has been questioned in relationship to Lamarck's hypothesis as it did not address the use and disuse of characteristics in response to the environment. Biologist Peter Gauthier noted that:

Can Weismann's experiment be considered a case of disuse? Lamarck proposed that when an organ was not used, it slowly, and very gradually atrophied. In time, over the course of many generations, it would gradually disappear as it was inherited in its modified form in each successive generation. Cutting the tails off mice does not seem to meet the qualifications of disuse, but rather falls in a category of accidental misuse... Lamarck's hypothesis has never been proven experimentally and there is no known mechanism to support the idea that somatic change, however acquired, can in some way induce a change in the germplasm. On the other hand it is difficult to disprove Lamarck's idea experimentally, and it seems that Weismann's experiment fails to provide the evidence to deny the Lamarckian hypothesis, since it lacks a key factor, namely the willful exertion of the animal in overcoming environmental obstacles.[20]

Science historian Michael Ghiselin also considers the Weismann tail-chopping experiment to have no bearing on the Lamarckian hypothesis:

The acquired characteristics that figured in Lamarck's thinking were changes that resulted from an individual's own drives and actions, not from the actions of external agents. Lamarck was not concerned with wounds, injuries or mutilations, and nothing that Lamarck had set forth was tested or "disproven" by the Weismann tail-chopping experiment.[17]

Neo-Lamarckism

Edward Drinker Cope

The period of the history of evolutionary thought between Darwin's death in the 1880s, and the foundation of population genetics in the 1920s and beginnings of modern evolutionary synthesis in the 1930s, is called the eclipse of Darwinism by some historians of science. During that time many scientists and philosophers accepted the reality of evolution but doubted whether natural selection was the main evolutionary mechanism.[21]

Among the most popular alternatives were theories involving the inheritance of characteristics acquired during an organism's lifetime. Scientists who felt that such Lamarckian mechanisms were the key to evolution were called neo-Lamarckians and included the British botanist George Henslow (1835–1925), who studied the effects of environmental stress on the growth of plants, in the belief that such environmentally-induced variation might explain much of plant evolution, and the American entomologist Alpheus Spring Packard, Jr., who studied blind animals living in caves and wrote a book in 1901 about Lamarck and his work.[22][23]

Also included were a number of paleontologists like Edward Drinker Cope and Alpheus Hyatt, who felt that the fossil record showed orderly, almost linear, patterns of development that they felt were better explained by Lamarckian mechanisms than by natural selection. Some people, including Cope and the Darwin critic Samuel Butler, felt that inheritance of acquired characteristics would let organisms shape their own evolution, since organisms that acquired new habits would change the use patterns of their organs, which would kick-start Lamarckian evolution. They considered this philosophically superior to Darwin's mechanism of random variation acted on by selective pressures. Lamarckism also appealed to those, like the philosopher Herbert Spencer and the German anatomist Ernst Haeckel, who saw evolution as an inherently progressive process.[22] The German zoologist Theodor Eimer combined Larmarckism with ideas about orthogenesis.[24]

With the development of the modern synthesis of the theory of evolution and a lack of evidence for a mechanism for acquiring and passing on new characteristics, or even their heritability, Lamarckism largely fell from favor. Unlike neo-Darwinism, the term neo-Lamarckism refers more to a loose grouping of largely heterodox theories and mechanisms that emerged after Lamarck's time, than to any coherent body of theoretical work.

Experiments

Charles-Édouard Brown-Séquard

In a series of experiments from 1869 to 1891, Charles-Édouard Brown-Séquard cut the sciatic nerve of the leg and spinal cord in the dorsal regions of guinea pigs, causing an abnormal nervous condition resembling epilepsy; these were then bred and produced epileptic offspring.[25] Although some scientists considered this evidence for Lamarckian inheritance, the experiments were not Lamarckian, as they did not address the use and disuse of characteristics in response to the environment.[26] The results from the experiment were not duplicated by other scientists.[27] One explanation for the results was that they show a transmitted disease, and not evidence for the inheritance of an acquired characteristic.[28] Brown-Séquard's experiments are now considered anomalous and alternative explanations have been suggested.[29]

The French botanist Gaston Bonnier, conducting experiments in the French Alps in 1884 and the Pyrenees in 1886, studied structural changes induced by growing plants at various altitudes and transplanting them to others. Bonnier believed he had proven acquired adaptive characteristics; however, he did not weed, cultivate, fertilize or protect his plant specimens from native vegetation. In the 1920s his experiments were analysed and attributed to genetic contamination rather than Lamarckian inheritance.[30]

In a series of experiments (in 1891, 1893 and 1895) on the action of light on the coloration of flatfish, the British marine biologist Joseph Thomas Cunningham (1859–1935) directed light upon the lower sides of flatfishes by means of a glass-bottomed tank placed over a mirror. He discovered the influence of light in producing pigments on the lower sides of flatfishes and gave his results a Lamarckian interpretation.[31][32][33] Other scientists wrote that Cunningham had received some definite results, but that they were open to more than one interpretation.[34] The geneticist William Bateson was not convinced that the cause of the increase in pigmentation was from the illumination. George Romanes wrote approvingly of Cunningham's interpretation.[35] Thomas Hunt Morgan criticized the experiments and did not believe the results were evidence for Lamarckism.[36]

In 1906, the philosopher Eugenio Rignano wrote a book, Sur La Transmissibilité Des Caractères Acquis, that argued for the inheritance of acquired characteristics.[37] He advanced a moderated Lamarckian hypothesis of inheritance known as "centro-epigenesis."[38][39] However, his views were controversial and not accepted by the majority in the scientific community.[40]

In a series of experiments from 1907 to 1910, William Lawrence Tower performed experiments on potato beetles which were said by Ernest MacBride to have provided evidence for the inheritance of acquired characteristics.[41] These were heavily criticized by William Bateson.[42] It was later suggested that his research may have been faked.[43] Tower claimed that the records of his experimental results had been lost in a fire.[44] The geneticist William E. Castle who visited Tower's laboratory was not impressed by the experimental conditions. He later concluded that Tower had faked his data. Castle found the fire suspicious and also Tower's claim that a steam leak in his greenhouse had destroyed all his beetle stocks.[45]

Experiments conducted by Gustav Tornier from 1907 to 1918 on goldfish and embryos of frogs and newts were supported by neo-Lamarckians such as Cunningham and MacBride as demonstrating the inheritance of acquired characteristics.[46][47] The abnormalities were interpreted as the result of an osmotic effect by other researchers.[48]

In the late 19th century, Frederick Merrifield exposed caterpillars and chrysalids to significantly high and low temperatures, and discovered permanent changes in some offspring's wing patterns. Swiss biologist Maximilian Rudolph Standfuss (1854–1917) led 30 years of intensive breeding experiments with European butterflies and after several generations, found similar preserved variations even generations after the cessation of exposing them to low temperatures.[49] Standfuss was a neo-Lamarckian and attributed the results of his experiments as direct changes to the environment.[50] In 1940, Richard Goldschmidt interpreted these results without invoking Lamarckian inheritance, and in 1998 Ernst Mayr wrote that results reported by Standfuss and others on the effects of abnormal temperatures on Lepidoptera are difficult to interpret.[51]

In 1910, the American zoologist Charles Rupert Stockard (1879–1939) tested the effects of alcohol intoxication on the offspring of pregnant guinea pigs. Stockard discovered that repeated alcohol intoxication in the guinea pigs produced defects and malformations in their offspring that was passed down to two or more generations. His results were challenged by the biologist Raymond Pearl who performed the same experiments with chickens.[52] Pearl discovered that the offspring of the chickens that had been exposed to alcohol were not defected but were healthy. He attributed his findings to the detrimental effects of alcohol only on the eggs and sperm which were already weak, the strong eggs and sperm were unaffected by alcohol intoxication. Pearl argued that his results had a Darwinian, not a Lamarckian explanation.[52]

The French zoologist Yves Delage in his book The Theories of Evolution (1912) reviewed experiments into Lamarckism concluded the evidence "is not of uniform value and is more or less open to criticism; very little of it is convincing... [due to] difficulties of experimentation and, above all, of interpretation."[53]

Paul Kammerer

In a series of experiments, Francis Bertody Sumner (1874–1945) reared several generations of white mice under different conditions of temperature and relative humidity.[54] Sumner discovered that the white mice at 20 °C to 30 °C developed longer bodies, tails and hind feet which were also transmitted to their offspring over a number of generations, however, later results were not entirely consistent and the experiments ended in uncertainty.[55]

Between 1918 and 1924, two American scientists Michael F. Guyer and Elizabeth A. Smith performed experiments in which fowl serum antibodies for rabbit lens-protein were injected into pregnant rabbits which resulted in defects in the eyes of some of their offspring that were inherited through eight generations.[56] Their experiments were criticized and were not repeated by other scientists.[57]

In the 1920s, experiments by Paul Kammerer on amphibians, particularly the midwife toad, appeared to find evidence supporting Lamarckism. However, his specimens with supposedly acquired black foot-pads were found to have been tampered with. In The Case of the Midwife Toad (1971), author and journalist Arthur Koestler surmised that the tampering had been done by a Nazi sympathiser to discredit Kammerer for his political views, and that his research might actually have been valid. However, most biologists believe that Kammerer was a fraud, and even among those who believe he was honest, most believe that he misinterpreted the results of his experiments.[58]

During the 1920s, Harvard University researcher William McDougall studied the abilities of rats to correctly solve mazes. He found that offspring of rats that had learned the maze were able to run it faster. The first rats would get it wrong 165 times before being able to run it perfectly each time, but after a few generations it was down to 20. McDougall attributed this to some sort of Lamarckian evolutionary process.[59] Oscar Werner Tiegs and Wilfred Eade Agar later showed McDougall's results to be incorrect, caused by poor experimental controls.[60][61] Peter Medawar wrote that "careful and extensive repetitions of McDougall's research failed altogether to confirm it. His work therefore becomes an exhibit in the capacious ill-lit museum of unreproducible phenomena."[62]

In the 1920s, John William Heslop-Harrison conducted experiments on the peppered moth, claiming to have evidence for the inheritance of acquired characteristics. Other scientists failed to replicate his results.[63][64] The Russian physiologist Ivan Pavlov claimed to have observed a similar phenomenon in white mice being subject to a conditioned reflex experiment involving food and the sound of a bell. He wrote that with each generation, the mice became easier to condition. In 1926, Pavlov announced that there had been a fatal flaw in his experiment and retracted his claim to have demonstrated Lamarckian inheritance.[65] Other researchers were also unable to replicate his results.[66]

In other experiments, Coleman Griffith (1920, 1922) and John Detlefson (1923, 1925) reared rats in cages on a rotating table for three months. The rats adapted to the rotating condition to such an extent that when the rotation was stopped they showed signs of disequilibration and other physiological conditions which were inherited for several generations.[67][68][69][70] In 1933, Roy Dorcus replicated their experiments but obtained different results as the rotated rats did not manifest any abnormalities of posture described by Griffith and Detlefson.[71] Other studies revealed that the same abnormalities could occur in rats without rotation if they were suffering from an ear infection thus the results were interpreted as a case of infection, not Lamarckian inheritance.[72]

In the 1930s, the German geneticist Victor Jollos (1887–1941) in a series of experiments claimed evidence for inherited changes induced by heat treatment in Drosophila melanogaster.[73] His experiments were described as Lamarckian. However, Jollos was not an advocate of Lamarckian evolution and attributed the results from his experiments as evidence for directed mutagenesis. American scientists were unable to replicate his results.[74]

The British anthropologist Frederic Wood Jones and the South African paleontologist Robert Broom supported a neo-Lamarckian view of human evolution as opposed to the Darwinian view. The German anthropologist Hermann Klaatsch relied on a neo-Lamarckian model of evolution to try and explain the origin of bipedalism. Neo-Lamarckism remained influential in biology until the 1940s when the role of natural selection was reasserted in evolution as part of the modern evolutionary synthesis.[75]

Herbert Graham Cannon, a British zoologist, defended Lamarckism in his 1959 book Lamarck and Modern Genetics.[76]

In the 1960s, "biochemical Lamarckism" was advocated by the embryologist Paul Wintrebert.[77]

Pierre-Paul Grassé

In the 1970s, Australian immunologist Edward J. Steele and colleagues proposed a neo-Lamarckian mechanism to try to explain why homologous DNA sequences from the VDJ gene regions of parent mice were found in their germ cells and seemed to persist in the offspring for a few generations. The mechanism involved the somatic selection and clonal amplification of newly acquired antibody gene sequences that were generated via somatic hypermutation in B-cells. The messenger RNA (mRNA) products of these somatically novel genes were captured by retroviruses endogenous to the B-cells and were then transported through the bloodstream where they could breach the soma-germ barrier and retrofect (reverse transcribe) the newly acquired genes into the cells of the germ line. Although Steele was advocating this theory for the better part of two decades, little more than indirect evidence was ever acquired to support it. An interesting attribute of this idea is that it strongly resembles Darwin's own theory of pangenesis, except in the soma to germ line feedback theory, pangenes are replaced with realistic retroviruses.[78] Regarding Steele's research, historian of biology Peter J. Bowler wrote, "his work was bitterly criticized at the time by biologists who doubted his experimental results and rejected his hypothetical mechanism as implausible."[79]

Neo-Lamarckism was dominant in French biology for more than a century. French scientists who supported neo-Lamarckism included Edmond Perrier (1844–1921), Alfred Giard (1846–1908), Gaston Bonnier (1853–1922) and Pierre-Paul Grassé (1895–1985).[80]

In 1987, Ryuichi Matsuda coined the term "pan-environmentalism" for his evolutionary theory which he saw as a fusion of Darwinism with neo-Lamarckism. He held that heterochrony is a main mechanism for evolutionary change and that novelty in evolution can be generated by genetic assimilation.[81][82] His views were criticized by Arthur M. Shapiro for providing no solid evidence for his theory. Shapiro noted that "Matsuda himself accepts too much at face value and is prone to wish-fulfilling interpretation."[82]

Since 1988, certain scientists have produced work proposing that Lamarckism could apply to single-celled organisms. A version of Lamarckian acquisition in higher order animals is still posited in certain branches of psychology, as, for example, in the Jungian racial memory.

Within the discipline of history of technology, Lamarckism has been used in linking cultural development to human evolution by classifying artefacts as extensions of human anatomy: in other words, as the acquired cultural characteristics of human beings. Ben Cullen has shown that a strong element of Lamarckism exists in sociocultural evolution.[83]

Ideological neo-Lamarckism

A form of Lamarckism was revived in the Soviet Union of the 1930s when Trofim Lysenko promoted Lysenkoism which suited the ideological opposition of Joseph Stalin to genetics. This ideologically driven research influenced Soviet agricultural policy which in turn was later blamed for crop failures.[84]

Neo-Lamarckian versions of evolution were widespread in the late 19th century. The idea that living things could to some degree choose the characteristics that would be inherited allowed them things to be in charge of their own destiny as opposed to the Darwinian view, which made them puppets at the mercy of the environment. Such ideas were more popular than natural selection in the late 19th century as it made it possible for biological evolution to fit into a framework of a divine or naturally willed plan, thus the neo-Lamarckian view of evolution was often advocated by proponents of orthogenesis.[85] According to Peter J. Bowler:

One of the most emotionally compelling arguments used by the neo-Lamarckians of the late nineteenth century was the claim that Darwinism was a mechanistic theory which reduced living things to puppets driven by heredity. The selection theory made life into a game of Russian roulette, where life or death was predetermined by the genes one inherited. The individual could do nothing to mitigate bad heredity. Lamarckism, in contrast, allowed the individual to choose a new habit when faced with an environmental challenge and shape the whole future course of evolution.[86]

Supporters of neo-Lamarckism such as George Bernard Shaw and Arthur Koestler claimed that Lamarckism is more humane and optimistic than Darwinism.[87]

Critical reception

George Gaylord Simpson in his book Tempo and Mode in Evolution (1944) claimed that experiments in heredity have failed to corroborate any Lamarckian process.[88] Simpson noted that neo-Lamarckism "stresses a factor that Lamarck rejected: inheritance of direct effects of the environment" and neo-Lamarckism is closer to Darwin's pangenesis than Lamarck's views.[89] Simpson wrote, "the inheritance of acquired characters, failed to meet the tests of observation and has been almost universally discarded by biologists."[90]

Botanist Conway Zirkle pointed out that Lamarck did not originate the hypothesis that acquired characters were heritable, therefore it is incorrect to refer to it as Lamarckism:

What Lamarck really did was to accept the hypothesis that acquired characters were heritable, a notion which had been held almost universally for well over two thousand years and which his contemporaries accepted as a matter of course, and to assume that the results of such inheritance were cumulative from generation to generation, thus producing, in time, new species. His individual contribution to biological theory consisted in his application to the problem of the origin of species of the view that acquired characters were inherited and in showing that evolution could be inferred logically from the accepted biological hypotheses. He would doubtless have been greatly astonished to learn that a belief in the inheritance of acquired characters is now labeled "Lamarckian," although he would almost certainly have felt flattered if evolution itself had been so designated.[91]

Peter Medawar wrote regarding Lamarckism, "very few professional biologists believe that anything of the kind occurs—or can occur—but the notion persists for a variety of nonscientific reasons." Medawar stated there is no known mechanism by which an adaption acquired in an individual's lifetime can be imprinted on the genome and Lamarckian inheritance is not valid unless it excludes the possibility of natural selection but this has not been demonstrated in any experiment.[92]

Martin Gardner wrote in his book Fads and Fallacies in the Name of Science (1957):

A host of experiments have been designed to test Lamarckianism. All that have been verified have proved negative. On the other hand, tens of thousands of experiments— reported in the journals and carefully checked and rechecked by geneticists throughout the world— have established the correctness of the gene-mutation theory beyond all reasonable doubt... In spite of the rapidly increasing evidence for natural selection, Lamarck has never ceased to have loyal followers.... There is indeed a strong emotional appeal in the thought that every little effort an animal puts forth is somehow transmitted to his progeny.[93]

According to Ernst Mayr, any Lamarckian theory involving the inheritance of acquired characters has been refuted as "DNA does not directly participate in the making of the phenotype and that the phenotype, in turn, does not control the composition of the DNA."[94] Peter J. Bowler has written that although many early scientists took Lamarckism seriously, it was discredited by genetics in the early twentieth century.[95]

Epigenetic Lamarckism

Illustration of a DNA molecule that is methylated at the two center cytosines. DNA methylation plays an important role for epigenetic gene regulation in development and disease.

Forms of 'soft' or epigenetic inheritance within organisms have been suggested as neo-Lamarckian in nature by such scientists as Eva Jablonka and Marion J. Lamb. In addition to 'hard' or genetic inheritance, involving the duplication of genetic material and its segregation during meiosis, there are other hereditary elements that pass into the germ cells also.[96] These include things like methylation patterns in DNA and chromatin marks, both of which regulate the activity of genes. These are considered Lamarckian in the sense that they are responsive to environmental stimuli and can differentially affect gene expression adaptively, with phenotypic results that can persist for many generations in certain organisms.[97]

Jablonka and Lamb have called for an extended evolutionary synthesis. They have argued that there is evidence for Lamarckian epigenetic control systems causing evolutionary changes and the mechanisms underlying epigenetic inheritance can also lead to saltational changes that reorganize the epigenome.[98]

Interest in Lamarckism has increased, as studies in the field of epigenetics have highlighted the possible inheritance of behavioral traits acquired by the previous generation.[96] A 2009 study examined foraging behavior in chickens as a function of stress:

Transmissions of information across generations which does not involve traditional inheritance of DNA-sequence alleles is often referred to as soft inheritance [99] or "Lamarckian inheritance."[100]

The study concluded:

Our findings suggest that unpredictable food access caused seemingly adaptive responses in feeding behavior, which may have been transmitted to the offspring by means of epigenetic mechanisms, including regulation of immune genes. This may have prepared the offspring for coping with an unpredictable environment.[100]

The evolution of acquired characteristics has also been shown in human populations who have experienced starvation, resulting in altered gene function in both the starved population and their offspring.[101] The process of DNA methylation is thought to be behind such changes.

In October 2010, further evidence linking food intake to traits inherited by the offspring were shown in a study of rats conducted by several Australian universities.[102] The study strongly suggested that fathers can transfer a propensity for obesity to their daughters as a result of the fathers' food intake, and not their genetics (or specific genes), prior to the conception of the daughter. A "paternal high-fat diet" was shown to cause cell dysfunction in the daughter, which in turn led to obesity for the daughter. Felicia Nowak, et al. reported at the Endocrine Society meeting in June 2013 that obese male rats passed on the tendency to obesity to their male offspring.[103]

Several studies, one conducted by researchers at Massachusetts Institute of Technology and another by researchers at the Tufts University School of Medicine, have rekindled the debate once again. As reported in MIT Technology Review in February 2009, "The effects of an animal's environment during adolescence can be passed down to future offspring ... The findings provide support for a 200-year-old theory of evolution that has been largely dismissed: Lamarckian evolution, which states that acquired characteristics can be passed on to offspring."[104] A report investigating the inheritance of resistance to viral infection in the nematode Caenorhabditis elegans suggests that small RNA molecules may be inherited in a non-Mendelian fashion and provide resistance to infection.[105]

A study (Akimoto et al. 2007) on epigenetic inheritance in rice plants came to the conclusion that "gene expression is flexibly tuned by methylation, allowing plants to gain or lose particular traits which are heritable as far as methylation patterns of corresponding genes are maintained. This is in support of the concept of Lamarckian inheritance, suggesting that acquired traits are heritable."[106] Another study (Sano, 2010) wrote that observations suggest that acquired traits are heritable in plants as far as the acquired methylation pattern is stably transmitted which is consistent with Lamarckian evolution.[107] Handel and Ramagopalan found that there is evidence that epigenetic alterations such as DNA methylation and histone modifications are transmitted transgenerationally as a mechanism for environmental influences to be passed from parents to offspring. According to Handel and Romagopalan "epigenetics allows the peaceful co-existence of Darwinian and Lamarckian evolution."[108]

In their book An Introduction to Zoology (2013), Joseph Springer and Dennis Holley wrote:

Lamarck and his ideas were ridiculed and discredited. In a strange twist of fate, Lamarck may have the last laugh. Epigenetics, an emerging field of genetics, has shown that Lamarck may have been at least partially correct all along. It seems that reversible and heritable changes can occur without a change in DNA sequence (genotype) and that such changes may be induced spontaneously or in response to environmental factors—Lamarck's "acquired traits." Determining which observed phenotypes are genetically inherited and which are environmentally induced remains an important and ongoing part of the study of genetics, developmental biology, and medicine.[109]

Eugene Koonin has written that the prokaryotic CRISPR system and Piwi-interacting RNA could be classified as Lamarckian and came to the conclusion that "Both Darwinian and Lamarckian modalities of evolution appear to be important, and reflect different aspects of the interaction between populations and the environment."[110]

A study in 2013 reported that mutations caused by a father's lifestyle can be inherited by his children through multiple generations.[111] A study from Lund University in Sweden showed that exercise changes the epigenetic pattern of genes that affect fat storage in the body.[112]

Commenting on this, Charlotte Ling explained:

The cells of the body contain DNA, which contains genes. We inherit our genes and they cannot be changed. The genes, however, have 'methyl groups' attached which affect what is known as 'gene expression' – whether the genes are activated or deactivated. The methyl groups can be influenced in various ways, through exercise, diet and lifestyle, in a process known as 'DNA methylation'.[113]

A 2013 study published in Nature Neuroscience reported that mice trained to fear the smell of a chemical called acetophenone passed their fear onto at least two generations.[114][115] The science magazine New Scientist commented on the study saying, "While it needs to be corroborated, this finding seems consistent with Lamarckian inheritance. It is, however, based on epigenetics: changes that tweak the action of genes, not the genes themselves. So it fits with natural selection – and may yet give Lamarck's name a sheen of respectability."[116]

Guy Barry wrote that Darwin's hypothesis pangenesis coupled with "Lamarckian somatic cell-derived epigenetic modifications" and de novo RNA and DNA mutations can explain the evolution of the human brain.[117]

Lamarckian elements also appear in the hologenome theory of evolution.[118]

Contrary views

Jerry Coyne has criticized Lamarckian claims of epigenetic inheritance.[119][120]

The significance of epigenetic inheritance to the evolutionary process is uncertain. Critics assert that epigenetic inheritance modifications are not inherited past two or three generations, so are not a stable basis for evolutionary change.[121][122] According to a recent review in 2015 "there are no reported epigenetic marks transmitted via the male germ line during more than three generations."[121]

The evolutionary biologist T. Ryan Gregory contends that epigenetic inheritance should not be considered Lamarckian. According to Gregory, Lamarck did not claim the environment imposed direct effects on organisms. Instead, Lamarck "argued that the environment created needs to which organisms responded by using some features more and others less, that this resulted in those features being accentuated or attenuated, and that this difference was then inherited by offspring." Gregory has stated that Lamarckian evolution in the context of epigenetics is actually closer to the view held by Darwin rather than by Lamarck.[6]

In a paper titled Weismann Rules! OK? Epigenetics and the Lamarckian Temptation (2007), David Haig writes that research into epigenetic processes does allow a Lamarckian element in evolution but the processes do not challenge the main tenets of the modern evolutionary synthesis as modern Lamarckians have claimed. Haig argued for the primary of DNA and evolution of epigenetic switches by natural selection.[123] Haig has also written there is a "visceral attraction" to Lamarckian evolution from the public and some scientists as it posits the world with a meaning, in which organisms can shape their own evolutionary destiny.[124]

American biologist Jerry Coyne has stated that "lots of studies show us that Lamarckian inheritance doesn’t operate" and epigenetic changes are rarely passed on to future generations, thus do not serve as the basis of evolutionary change.[125] Coyne has also written:

Lamarckism is not a “heresy,” but simply a hypothesis that hasn’t held up... If “epigenetics” in the second sense is so important in evolution, let us have a list of, say, a hundred adaptations of organisms that evolved in this Larmackian way as opposed to the old, boring, neo-Darwinian way involving inherited changes in DNA sequence... I can’t think of a single entry for that list.[126]

Thomas Dickens and Qazi Rahman (2012) have written epigenetic mechanisms such as DNA methylation and histone modification are genetically inherited under the control of natural selection and do not challenge the modern synthesis. Dickens and Rahman have taken issue with the claims of Eva Jablonka and Marion J. Lamb on Lamarckian epigenetic processes.[127]

Edith Heard and Robert Martienssen (2014) in a Cell review were not convinced that epigenetics has revived Lamarckism as there is no evidence epigenetic changes are passed on to successive generations in mammals. They concluded the characteristics that are thought to be the result of epigenetic inheritance may be caused by other factors such as behavioral changes, undetected mutations, microbiome alterations or the transmission of metabolites.[128]

In 2015, Khursheed Iqbal and colleagues discovered that although "endocrine disruptors exert direct epigenetic effects in the exposed fetal germ cells, these are corrected by reprogramming events in the next generation." Molecular biologist Emma Whitelaw has cited this study as an example of evidence disputing Lamarckian epigenetic inheritance.[129] Another critic recently argued that bringing back Lamarck in the context of epigenetics is misleading, commenting, "We should remember [Lamarck] for the good he contributed to science, not for things that resemble his theory only superficially. Indeed, thinking of CRISPR and other phenomena as Lamarckian only obscures the simple and elegant way evolution really works."[130]

See also

References

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