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1900 1902 1904 1908 1929 1932 1938 1940 1944 1947 1956 1960 1961 1963 1966 1974
Herrera establishes The National School (19321933) Taboada The Mexican The Mexican Institute of The Mexican National The International The University of
the first general of Agriculture is attends university courses Department of Agronomical Research Institute of Agronomical Maize and Wheat Chapingo
biology course in established. at Cornell and Minnesota. Experimental is established. Research is set up. Improvement becomes
Mexico. Stations is Center is formed. autonomous.
(19321933) The National established. de Garay initiates the Genetics and
Polytechnic Institute is formed. Radiobiology Program in Mexico.
that guided plant-breeding practices before Mexico followed a fairly typical course for Early Mendelism in Mexico
the establishment of Mendelism had been Latin American countries, in that genetics In some ways the history of genetics in
unreliable, but Mendelian hybridization was first applied to agriculture. The key Mexico might be seen as a typical example
rectified the situation and new varieties of features that allowed genetics to develop in of the emergence of scientific research in
corn, wheat, rice and other crops were intro- Mexico are also visible in Brazil, where the ex-colonial countries. But the emergence
duced. Mendelians supported the idea that discipline was institutionalized in the 1920s of genetics in Mexico had distinctive fea-
hybridization provides almost infinite pos- and 1930s with support from the Rockefeller tures that were largely determined by the
sibilities for crop improvement, and that the Foundation. confluence of social and political factors,
recombination of characters can be predicted the proximity to and interest of the United
in a mathematically precise manner14. Brazils response to genetic discoveries. In States, and the pervasiveness of religious
During the same period the chromo- Brazil, genetics was first taught in univer- beliefs and influence of the Catholic
some theory of inheritance was developed, sities in the 1920s as part of agricultural Church. The earliest investigations of bio-
mostly under the leadership of Thomas programmes by Carlos Teixeira Mendes, logical inheritance by Mexican scientists
Hunt Morgans research group at Columbia Octavio Domnguez and Salvador de preceded modern Mendelism, and were
University15. In the 1920s and 1930s numer- Toledo Piza. Andr Dreyfus introduced instead motivated by the interest of biolo-
ous advances were made, including the genetics, also in the 1920s, in the medical gists and physicians in the role of heredity
development of the first gene maps and school of So Paulo. He later taught courses in determining human traits and human
the demonstration that mutations could be in genetics and evolution at the University
induced experimentally16. of So Paulo, which was established with
support from the Rockefeller Foundation
Mexicos response to genetic discoveries. In in the early 1930s. The eminent population
Mexico, a predominantly agricultural coun- geneticist Theodosius Dobzhansky was
try, genetic research was guided during the invited in 1942 to teach as a visiting profes-
first half of the twentieth century by its appli- sor in Dreyfus department, and to initiate
cations to agriculture. In the 1920s Mexican a research group there.
agriculture became negatively affected by The institutionalization of genetics in
the armed conflicts associated with the Brazil can be traced to the foundation of
revolutionary movement that had pervaded the Department of Biology by Dreyfus and
the country since 1911. Agricultural activity Dobzhansky in the University of So Paulo.
was devastated, physically and socially, and In 1948 and 1955 Dobzhansky returned while
farming practices significantly deteriorated. on sabbatical leave to initiate an ambitious
Agricultural research was an area that could project. This involved the study of genetic
significantly contribute towards an urgently variability in natural populations of groups
needed agricultural recovery. Previous revo- of two neotropical species that are related
lutionary governments had expressed inter- to Drosophila willistoni and Drosophila
est in this recovery, but it was not until the prosaltans, and the investigation of chromo-
late 1930s that plant breeders became aware somal polymorphisms and of the process of
of Mendelism and used it as a means to trans- speciation in species of the D. willistoni group.
form the art of plant breeding into a rigorous By 1956 about a dozen centres of genetic
scientific enterprise, with the improvement research had been created, and diverse research
of seeds for crops such as maize, sesame, programmes were developed, including Figure 1| Alfonso Luis Herrera circa 1915. Image
potato and wheat. The history of genetics in human, plant and developmental genetics17. courtesy of Jorge Llorente, UNAM.
health. This research also addressed envi- Agriculture in Chapingo, and he wrote the hybrids that were obtained. Finally, he used
ronmental influences on hereditary diseases first textbook of general genetics, Apuntes all successful hybrid combinations to retain
and malformations, such as the consumption de Gentica (Notes on Genetics) in 1938 as much genetic diversity as possible.
of certain drugs or foods, and the influence of REF. 22. By creating stabilized varieties of maize,
marriages between relatives. His research focused on solving the Taboada was seeking to solve a problem that
In 1902 Alfonso Luis Herrera (FIG. 1), a technical and economic problems faced by the poorest farmers had to deal with: the
prominent Mexican scientist, established small farmers share-croppers, peasants need to purchase seeds at the beginning of
the first general biology course in Mexico and indigenous communities. In the 1930s, every planting season. However, the research
at the Escuela Normal para Maestros however, his achievements had a limited results obtained by the OCE and the IIA did
(Teacher Training College) and, in 1904, he impact. The improved seeds he obtained not have a significant effect on the Mexican
published the textbook Nociones de Biologa were only supplied to farmers who were liv- agricultural economy. This was mainly
(Concepts of Biology)18. Herreras book and ing in the vicinity of the experimental station because, although his work was a significant
teaching represent the first serious intro- where his research was done, as there was no achievement in Mexican agriculture, it was
duction of modern biology and Darwinism infrastructure for their wider distribution. directed towards helping small farmers. In
to Mexico. Herrera saw biology as an inde- Taboada was appointed as director addition, as is discussed in the following sec-
pendent discipline that seeks to explain of the Office of Experimental Stations tion, Taboada was hindered by institutional
natural phenomena of life, rather than an (OCE), the first experimental agricultural policies and the limited financial support of
introduction to concepts and applications government agency in Mexico, which was the Mexican government.
of agriculture or medicine. In Nociones de created in 1940. The OCE was endowed with
Biologa, Herrera refers to Mendels Laws ten experimental stations in different states The Rockefeller Foundation in Mexico
and De Vries Laws, but considers them of the country, where researchers crossed and The activities of the Rockefeller Foundation
primarily from an evolutionary perspec- tested varieties of maize, rice, sesame, wheat, in Latin America began early in the twen-
tive. The book also introduces the concept cotton, sugar cane, bean, olive, potato, hemp tieth century. When it was established, the
of PLASMOGENY and the study of the processes and guayule (a source of natural rubber). Rockefeller Foundation identified world-
involved in organic evolution. Many experiments were designed to solve wide health and economic welfare among its
Herrera was criticized because his approach agricultural problems that were relevant to objectives, and its early campaigns focused
was at odds with the urgent social needs of small farmers, such as PRECOCITY, productiv- on public health and medicine (hookworm
the time, which called for improved eco- ity, resistance to disease, and adaptation to in Brazil, 1916; yellow fever in Mexico, 1923;
nomic development and basic health, instead the local climate and soil. and malaria in Brazil, 1938). After 1928 the
of advancing theories about the origin and In 1947 the OCE became the Institute of Rockefeller Foundation also emphasized sci-
evolution of life. His opponents insisted that Agronomical Research (IIA), and Taboada entific development, including research and
practical studies should have priority over remained as director until 1960. An important education. The activities of the Rockefeller
theoretical concerns. Moreover, Herreras contribution of the IIA to Mexican agriculture Foundation in Europe mostly ceased dur-
evolutionary ideas were in conflict with reli- was the development of so-called stabilized ing the Second World War, opening up new
gious and social prejudices held by political varieties of local varieties of maize23. To do possibilities in Latin America. The agency
and religious sectors that had considerable this, Taboada first obtained pure lines with was particularly interested in promoting
social influence19. few agronomical disadvantages and good agriculture, because poor nutrition was a
The ideas about heredity that had been combinatorial fitness. He then selected the contributing factor to handicapping the
introduced at the end of the nineteenth cen- most productive lines through repeated economic development of Latin American
tury by the medical community did not have crosses and the subsequent assessment of the countries24.
any significant role in Mexico in the first
decades of the twentieth century not even
among the early biologists of the country,
who lacked an interest in hereditary theo-
ries that failed to incorporate Mendelism at
their base.
ated the Office of Special Studies (OEE), eth century, it was not until the second half of TRANSFORMATION
which was initially directed by North the century that genetics was institutionalized. Alteration of the genome of bacterial or other cells by
American researchers who collaborated with Basic research and research that was directed their uptake of DNA purified from other organisms.
which Mexico participated, against nuclear supported by the IAEO. Between 1960 and communication and knowledge exchange
tests in the atmosphere. 1970 more than 25 scientists were trained in between individual scientists, as well as with
The Genetics and Radiobiology Program some of the worlds best institutions, includ- national and foreign societies.
was established to enhance public health ing the Universities of California (Berkeley), The most significant change to the Genetics
through physical and mental improvement Chicago, Rockefeller and Wisconsin in and Radiobiology Program occurred in 1973
and sickness prevention, by investigation of the United States; Cambridge University, when the programme was incorporated into
the factors that intervene (favourably or unfa- University College London and the University the National Institute for Nuclear Research
vourably) in the biological inheritance of a of Newcastle-Upon-Tyne in England; and the in Salazar and its size was reduced to include
population.26 The programme consisted of six Hpital des Enfants Malades in France. only four laboratories: the Plant Genetics,
sections or laboratories. The most important The educational efforts of the pro- Microbial Genetics, Drosophila and Human
of these was the Drosophila laboratory, which gramme during its first 10 years were Genetics Laboratories. This reduction was
focused on conventional genetics experimen- important for the consolidation of genet- deemed necessary because by this time other
tation and the measurement of mutation ics in Mexico. Courses were taught at the institutions were carrying out similar inves-
rates, including those in irradiated stocks. School of Sciences at UNAM (the huge tigations and there was pressure to reduce
During the 1960s research evolved in several National Autonomous University in the financial resources that were committed
directions, with the aim that genetic research Mexico City) and included modules such to genetics research. Between 1960 and 1980
at the National Commission of Nuclear as advanced genetics, genetics of develop- the programme published nearly 140 papers
Energy should achieve competitiveness on ment, and genetics of human populations in national and international journals.
a worldwide scale. In 1965 and 1966 the and evolution. Courses were also taught in
programme added the Aquatic Invertebrate other institutions such as the Autonomous Genetics today: a brief prcis
Radiobiology section, which focused on University of Puebla and the National In the final decades of the twentieth century,
compounds that protect against the effects of Commission of Nuclear Energy. genetics in Mexico advanced at fast pace
radiation in planarians (flatworms), and the de Garay founded the Mexican Genetics and made important contributions to world
Molecular Genetics laboratory, which inves- Society in 1966, coinciding with the hun- science, particularly in four subdisciplines:
tigated the genetic mechanisms that operate dredth anniversary of the publication of breeding genetics, molecular genetics,
in microorganisms, and the consequences of Mendels classic paper29. The Society was human genetics and population genetics.
radiation and of radioprotective substances at founded with only a dozen members, and The International Maize and Wheat
the molecular level28. de Garay was its first President, holding the Improvement Centre (CIMMYT), created in
de Garay encouraged the investigators post until 1979. The goals of the Society 1963, was primarily a product of the involve-
who were involved in the programme to make were to promote genetic research, the teach- ment of the Rockefeller and Ford Foundations,
at least short visits to foreign universities, ing and popularization of genetics, and and was a by-product of the research carried
out by the OEE and the INIA. CIMMYT is a
leader in global maize and wheat innovation,
Box 1 | The Genetics and Radiobiology Program and in the use of knowledge and technol-
ogy to increase food security, improve the
This programme was initiated in 1960 with its laboratories located in an apartment building in productivity and profitability of farming
Mexico City. It consisted of six researchers, including Alfonso Len de Garay as director,
systems, and sustain natural resources. Its
Rodolfo Flix Estrada as chief of the Drosophila section, and four scientists who had obtained
agricultural research programme, and the
their B.A. degrees in biology in 1960, as well as a technician, a secretary and a service assistant.
Green Revolution that emerged from it,
The programme started as an activity of the Mexican National Commission of Nuclear Energy,
with the primary mission of investigating the genetic effects of atomic radiation.
have significantly improved agricultural
The Drosophila laboratory was the main experimental component of the programme. technology and production throughout
Numerous mutant stocks were obtained from laboratories throughout the world. Wild-type the developing world. CIMMYT is broadly
and mutant flies were exposed to various doses of X-irradiation or RADIOISOTOPES, and the considered a model of how technical assist-
mutagenic effects on the genome were estimated by examining the progeny. The mutant stocks ance and research support should flow from
were also used for genetics teaching. All investigators were required to attend annual courses industrial to developing countries. This insti-
run by the programme on genetics, radioisotopes and nuclear instrumentation. tution is part of an international consortium
After 2 years of activity, the programme was restructured into six laboratories: human (the Consulting Group on International
genetics, Drosophila genetics, mammalian genetics, radiation genetics and biochemistry, Agricultural Research, CGIAR) that sup-
quantitative genetics, and statistics. Research was extended beyond the study of individual gene ports research on the main crops all around
effects in Drosophila to the investigation of the damaging effects caused by X-rays and ozone on the world.
human tissue culture cells, and on processes such as meiosis and mitosis during Drosophila Two distinguished Mexican scientists
development. New facilities were created for human tissue culture, mammalian histology and and the institutions in which they work
human chromosome analysis. In 1962 the programme also initiated research on human exemplify the enormous strides taken by
variation and anthropology. Mexican research in molecular genet-
International personalities were invited to visit and participate in the different components of ics. While working in the United States,
the programme. In 1965 Louis Levine, who was visiting from City College in New York, Francisco Bolvar made important contri-
recommended the establishment of a policy that would require young Mexican geneticists in butions to the development of methods for
the programme to spend several years abroad for research and training. He also suggested that
producing human recombinant proteins in
three new research programmes should be established: molecular genetics, developmental
bacteria30, and he was also responsible for
genetics and behavioural genetics. Other well-known scientists who were invited by de Garay
developing new molecular tools for cloning
were Francisco J. Ayala in 1968 and Theodosius Dobzhansky in 1973.
and expressing DNA in Escherichia coli31.
Another Mexican, Luis Herrera Estrella32, Conclusions 5. Stepan, N. Beginnings of Brazilian Science: Oswaldo
Cruz, Medical Research and Policy, 18901920 (Science
who worked in Belgium, significantly Two features of Mexican society, politics and History Publications, New York, 1981).
improved our understanding of genetic history contributed to the late emergence 6. Lafuente, A. & Sala Catal, J. Ciencia colonial y roles
profesionales en la Amrica Espaola del Siglo XVIII.
TRANSFORMATION in plants. The research and development of genetics in Mexico. The Quipu 6, 387403 (1989) (in Spanish).
institutions in which they now work the first was economic underdevelopment and 7. Vessuri, H. in The Uncertain Quest. Science, Technology
Institute of Biotechnology in Cuernavaca the resulting scarcity of scientists, condi- and Development (eds Salomon, J. J., Sagasti, F. R. &
Sachs-Jeantet, C.) 168200 (United Nations Univ. Press,
and the C entro de Investigaciones tions that were shared a century ago by other New York, 1994.
Avanzadas (CINVESTAV) in Irapuato of the developing countries. The other feature was 8. Home, R. W. & Kohlstedt, S. G. (eds) International
Science and National Scientific Identity: Australia
UNAM together employ approximately distinctive: the ideological and religious con- between Britain and America (Kluwer Academic,
300 scientists that work on various aspects victions of a deeply Catholic population, who Dordrecht, 1991).
9. Petitjean, P. in Science and Empires: Historical Studies
of plant, animal and bacteria molecular biol- saw biological evolution and research on the about Scientific Development and European Expansion
ogy and biotechnology. These institutions genetic causation of human disease as con- (eds Petitjean, P., Jami, C. & Moulin, A. M.) (Kluwer
are often visited by scientists from Europe, trary to universally held beliefs concerning Academic, Dordrecht, 1992).
10. Palladino, P. & Worboys, M. Science and imperialism. Isis
the United States and elsewhere, and their Gods creation. 84, 91102 (1993).
researchers have established collaborations The history of genetics in Mexico also 11. Palladino, P. Between craft and science: plant breeding,
Mendelian genetics, and British universities, 19001920.
with scientists throughout the world. shows how a technologically developed coun- Technol. Cult. 34, 300323 (1993).
In Mexico, medical research is mostly try such as the United States can significantly 12. Paul, D. B. & Kimmelman, B. A. in The American
Development of Biology (eds Rainger, R., Benson, K. &
done in government hospitals, where human contribute to the transformation of a scientifi- Maienschein, J.) 281310 (Univ. Pennsylvania Press,
genetics research particularly blossomed. cally backward enterprise as Mexico was in Philadelphia, 1988).
Research is also carried out in health-related the 1930s and 1940s into a country with 13. Kimmelman, B. A. The American Breeders Association:
genetics and eugenics in an agricultural context,
institutes by distinguished scientists, such world-class scientific programmes and insti- 19031913. Soc. Stud. Sci. 13, 163204 (1983).
as Antonio Velzquez33 and Rubn Lisker34, tutions, through a combination of expertise 14. Kimmelman, B. A. A progressive era discipline:
genetics at American agricultural colleges and
who pioneered the genetic characterization and financial support. experimental stations, 19001920. Thesis, Univ.
of the numerous and distinct indigenous The proletarian ideals of the Mexican Pennsylvania (1987).
15. Morgan, T. H., Sturtevant, A. H., Muller, H. J. &
Mexican populations. Considerable research Revolution (19101917) led to agricultural Bridges, C. B. The Mechanism of Mendelian Heredity
is now focused on genetic markers for some practices that were associated with the redis- (Holt and Co., New York, 1915).
diseases that are important in Mexico, such tribution of farms from large property own- 16. Dunn, L. C. A Short History of Genetics (McGraw-Hill,
New York, 1965).
as diabetes, cancer and cardiovascular disor- ers to the peasants who cultivated the farms. 17. Glick, T. F. in Missionaries of Science. The Rockefeller
ders. In Mexico City and Guadalajara alone, Proximity to the United States facilitated the Foundation and Latin America (ed. Cueto, M.) 149164
(Indiana Univ. Press, Bloomington, 1994).
approximately 100 scientists work on human interest of the Rockefeller, Ford and other 18. Herrera, A. L. Nociones de Biologa (Imprenta de la
genetics. Foundations in developing agricultural tech- Secretara de Fomento, Mexico, 1904; facsimile edn,
Universidad Autnoma de Puebla, Mexico, 1992) (in
From the beginning, population genet- nologies and practices that were suitable for Spanish).
ics was a significant area of research of the the developing world, which led to the Green 19. Ledesma, I. & Barahona, A. The institutionalization of
Genetics and Radiobiology Program that was Revolution and contributed to the establish- biology in Mexico in the early 20th century. The conflict
between Alfonso Luis Herrera (18681942) and Isaac
led by de Garay, and was primarily stimu- ment of genetics research and teaching. Ochoterena (18851950). J. Hist. Biol. 36, 285307
lated by two developments. The first involved The international ban against atmospheric (2003).
20. Anonymous. Los agrnomos Mexicanos. Revista
the genetic study of athletes participating nuclear testing, which was joined by Mexico, Panorama Agrcola Nacional (PANAGRAL) 7, 89 (1963)
in the World Olympics held in Mexico in and the selection of de Garay to lead related (in Spanish).
21. Instituto Nacional de Investigaciones Agrcolas.
1968. The second research project emerged scientific research, were contingent factors Edmundo L. Taboada Ramrez: una Semblanza,
in 1973 from discussions between de Garay that accounted for the rapid institutionali- 19061983 (Instituto Nacional de Investigaciones
and Dobzhansky, on the population genet- zation of genetics research and teaching in Agrcolas, Mexico, 1985) (in Spanish).
22. Taboada, E. Apuntes de Gentica (Escuela Nacional de
ics of Mexican Drosophila. Dobzhansky was Mexico in the past few decades. Agricultura/Chapingo, Mexico, 1938) (in Spanish).
seeking to understand the ecological basis Ana Barahona is at the Departamento de Biologa
23. Secretara de Agricultura y Ganadera. Informe de
Labores, 19511952 (Secretara de Agricultura y
of genetic variation in natural populations Evolutiva, Facultad de Ciencias, UNAM, Zapata Ganadera, Mexico, 1952) (in Spanish).
in Drosophila pseudoobscura, and the rela- 69, Col. Miguel Hidalgo, Tlalpan 14410, Mexico. 24. Cueto, M. Introduction in Missionaries of Science. The
Rockefeller Foundation and Latin America (ed. Cueto, M.)
tionships between the amount of genetic Francisco J. Ayala is at the Department of Ecology (Indiana Univ. Press, Bloomington, 1994).
variation present in a population and its and Evolutionary Biology, University of 25. Harrar, J. Q. The Agricultural Program of the
California, Irvine, 321 Steinhaus Hall, Irvine, Rockefeller Foundation (Rockefeller Foundation, New
rate of evolution a project that yielded California 92697-2525, USA. York, 1956).
numerous research articles between 1974 26. de Garay, A. L. Programa de Gentica y Radiobiologa.
Correspondence to A.B. and F.J.A.
and 1995 REFS 35,36. e-mails: abe@hp.fciencias.unam.mx;
Informe de Labores 1960 (Comisin Nacional de
Energa Nuclear, Archivo de Informacin, Biblioteca del
Recent developments include a B.Sc. fjayala@uci.edu ININ, Mexico, 1960) (in Spanish).
degree programme in genomics, which doi:10.1038/nrg1705 27. Barahona, A., Pinar, S. & Ayala, F. J. La Gentica en
Mxico. Institucionalizacin de una Disciplina
was initiated in 2003 through a collabora- Published online 20 September 2005
(Universidad Nacional Autnoma de Mxico, Mexico,
tion of UNAMs new Center for Genomic 1. Basalla, G. The spread of western science. Science 156, 2003) (in Spanish).
Sciences and the Institute of Biotechnology 611622 (1967). 28. de Garay, A. L. Programa de Gentica y Radiobiologa.
2. Sagasti, F. & Guerrero, M. El Desarrollo Cientfico y Informe de Labores 1965 (Comisin Nacional de Energa
in Cuernavaca. In addition, the Mexican Tecnolgico en Amrica Latina (Instituto para la Integracin Nuclear, Archivo de Informacin, Biblioteca del ININ,
Congress recently approved the Biosafety de Amrica Latina, Buenos Aires, 1974) (in Spanish). Mexico, 1965) (in Spanish).
3. Inkster, I. Scientific enterprise and the colonial model: 29. Sociedad Mexicana de Gentica. Estatutos de la
Law for Genetically Modified Organisms, and observations on Australian experience in historical Sociedad Mexicana de Gentica, A. C. (Sociedad
legislated the creation of a National Institute context. Soc. Stud. Sci. 15, 677704 (1985). Mexicana de Gentica, Mexico, 1966) (in Spanish).
4. Stafford, R. in Australian Science in the Making 30. Bolivar, F. et al. Construction and characterization of new
of Genomics and Health, which began its (ed. Home, R. W.) 69101 (Cambridge Univ. Press, cloning vehicles. II. A multipurpose cloning system. Gene
activities in 2005. Cambridge, 1988). 2, 95113 (1977).
31. Itakura, K. et al. Expression in Escherichia coli of a 36. Olvera, O. et al. Chromosomal and behavioral Theories of ageing
chemically synthesized gene for the hormone studies of Mexican Drosophila. III. Inversion
somatostatin. Science 198, 10561060 (1977). polymorphism of D. pseudoobscura. J. Hered. 76, In this section, we will briefly discuss how
32. Herrera-Estrella, L., Depicker, A., Van Montagu, M. & 258262 (1985). each of the different theories of ageing fits
Schell, J. Expression of chimaeric genes transferred into
plant cells using a Ti-plasmid-derived vector. Nature 303, Acknowledgements the data that have been generated by studies
209213 (1983). We thank Daniel Piero and two anonymous referees for their of lifespan in model systems. Although these
33. Velzquez-Arellano, A. Cederbaum, S., comments on previous versions.
Salamanca-Gmez, F., Rodrguez, M. &
theories clearly provide different views on
Competing interests statement how and why ageing and death occur, they
Velzquez, A. New frontiers in human genetics and their The authors declare no competing financial interests.
implications. Gaceta Mdica Mexicana 122, also overlap.
123134 (1986).
34. Lisker, R. Estructura Gentica de la Poblacin Mexicana Online links
(Salvat Mexicana de Ediciones, Mexico, 1981) (in Spanish).
FURTHER INFORMATION The free radical theory. The free radical
35. Olvera, O. et al. Population genetics of Mexican
Drosophila. VI. Cytogenetic aspects of the inversion
Francisco J. Ayalas homepage: http://www.faculty. theory of ageing proposes that the reactive
uci.edu/profile.cfm?faculty_id=2134&name=Francisco
polymorphism in D. pseudoobscura. Evolution 33, %20J.%20Ayala oxygen species that are produced as part of
381395 (1979). Access to this interactive links box is free online.
normal metabolism cause ageing by slowly
damaging macromolecules, organelles and
cells10,11. It is now widely accepted, and we
agree, that free radicals are a principal medi-
OPINION
ator of ageing10,11. However, a fundamental
question to be addressed is whether free
radicals and other insults are the primary
Programmed and altruistic ageing cause of ageing, or whether ageing and death
occurs mostly after a putative programme
that regulates protection, repair and replace-
Valter D. Longo, Joshua Mitteldorf and Vladimir P. Skulachev ment systems becomes less efficient. We
discuss this issue in later sections.
Abstract | Ageing is widely believed to and other toxic species following the The disposable soma theory. It was August
be a non-adaptive process that results decline of the force of natural selection Weismann who suggested that chemical
from a decline in the force of natural and the consequent decline in protection and mechanical damage is, in principle,
selection. However, recent studies in and repair mechanisms with increasing reparable to an arbitrarily high standard of
Saccharomyces cerevisiae are consistent age 3,4 . However, a series of pioneering faithfulness12. However, theories of meta-
with the existence of a programme genetic studies that were carried out in bolic trade-off offer an explanation of why
of altruistic ageing and death. We yeast, worms, flies and mice over the past molecular repair mechanisms might have
suggest that the similarities between 15 years have shown that lifespan can be limited effectiveness. The disposable soma
the molecular pathways that regulate extended by threefold or more through theory takes these metabolic trade-offs
ageing in yeast, worms, flies and mice, mutations that force entry into phases that into account. According to this theory, the
together with evidence that is consistent are normally entered under conditions of repair of stochastic damage requires caloric
with programmed death in salmon and starvation5,6. These findings indicate that a energy, and competing metabolic demands
other organisms, raise the possibility that genetic programme might regulate the level for this energy have forced natural selection
programmed ageing or death can also of protection against stochastic damage, into an optimization process in which com-
occur in higher eukaryotes. and therefore the length of time an organ- promises between longevity and growth or
ism remains healthy. Another possibility reproduction are inherent13. Consistent with
Ageing describes all of the time-dependent and the focus of this review is that a this theory, trade-offs that include decreased
changes that occur in the molecules, cells programme can promote ageing and death fertility or growth are observed in most but
and tissues of an organism, whereas senes- for altruistic reasons (the programmed not all long-lived mutant organisms5.
cence can be defined as the subset of those and altruistic ageing theory). There are In disagreement with this theory is the
changes that negatively affect the functions two possible explanations for such altruis- observation that caloric restriction, and not
of the organism 1 . However, because the tic behaviour one explanation is that it increased caloric intake, has been observed
term ageing is more widely used than benefits closely related organisms that have to extend lifespan in a diverse range of spe-
senescence to define detrimental age- acquired mutations that increase their abil- cies14. However, it is possible that a reduction
dependent changes, we will use ageing ity to grow and survive, the other is that it in nutrient availability increases rather than
throughout this review1,2. Ageing occurs in benefits the group as a whole. decreases the energy that is available for
organisms that range from yeast to humans, Recent studies of the unicellular organ- somatic maintenance by saving the energy
but also in non-living systems such as ism Saccharomyces cerevisiae raise the that is normally invested in growth and
automobiles. Do organisms become rusty controversial possibility that programmed reproduction14,15. Further studies are neces-
and age like cars or is there a genetic pro- and altruistic ageing might occur, and sary to determine whether the disposable
gramme that guarantees that a specific age that this might be an adaptive process that soma theory might explain ageing, alone or
is reached? benefits small sub-populations of closely in combination with other theories.
Gerontologists widely support theories related mutants 79 . Here we review the
of ageing that are based on the non-adap- programmed and altruistic ageing theory The antagonistic pleiotropy theory. There is
tive accumulation of stochastic damage to and the recent experimental evidence that also the possibility of purely genetic trade-offs,
macromolecules that is caused by oxygen supports it. as described by the antagonistic pleiotropy