You pass to your children not only the contents of your genetic code.
The idea that all inherited traits of living beings are encoded in genes has been a fundamental dogma of genetics and evolutionary biology for many years. But this assumption constantly had to exist in an unpleasant neighborhood with the inconvenient discoveries of empirical research. And in recent years, complications have accumulated at an exponential rate under the weight of new discoveries.
Classical genetics makes a fundamental distinction between the "
genotype " (that is, the set of genes transferred by an individual, which he can pass on to descendants) and the "
phenotype " (temporary state of the body, bearing the imprint of his environment and his experience, whose features are not transmitted to descendants). It is assumed that only genetically predetermined properties can be inherited - that is, transferred to descendants - because inheritance passes exclusively through the transfer of genes. However, it was shown that, in violation of the genotype / phenotype dichotomy, lines of genetically identical animals and plants may experience
variations in inheritance and respond to natural selection.
Conversely, genes are not able to explain why relatives have very similar complex properties and diseases - this problem was called “lacking heritability”. Studies of genomes have not yet been able to determine the genes, whose influence in the amount can explain the observation of the heritability of a variety of properties, from “family” diseases to such inherited traits as growth. In other words, although relatives demonstrate the similarity of phenotypes, they have very few common
alleles , which is why the genetic basis of this feature is not clear. Lack of heritability may occur due to complex gene interactions (
epistasis ), since such interactions are difficult to take into account when studying the genomes in their entirety. It may also appear due to the non-genetic nature of the inherited variation, especially if it is generated by the environment.
However, if the individual's own genotype does not seem to be responsible for some of its features, it turned out that the genes of the parents affect the properties of the descendants who did not inherit these genes. Moreover, studies of plants, insects, rodents and other organisms show that the environment surrounding the individual and his life experience - diet, temperature, parasites, social interaction - can influence the characteristics of his descendants. Studies of our species suggest that we are no different in this regard. Some of the discoveries clearly fit the definition of “inheritance of acquired properties” - a phenomenon which, according to the famous analogy that appeared before Google, is just as impossible as if a telegram in Chinese sent from Beijing would have arrived in London already translated into English tongue. But today, such phenomena are regularly reported in scientific journals. And just as the Internet and instant translation have revolutionized the transmission of messages, discoveries in molecular biology turn over ideas about what can and cannot be passed from generation to generation.
Biologists are faced with the monumental challenge of recognizing a rapidly accumulating zoo of discoveries that violate ingrained perceptions. You can get an idea of the growing dissonance between theory and evidence by reading a recent review of these studies, and then the introductory chapter of any biology textbook for students. In the generally accepted concept of heredity, which states that inheritance is controlled exclusively by genes, and rejects the possibility that the influence of the environment and life experience can be passed on to descendants, something is clearly lacking.
If some non-genetic variability is inherited, then it turns out that this variability can react to natural selection and lead to the appearance of phenotypic changes in generations in the absence of genetic changes. Such changes do not fit into the standard genetic definition of evolution, bounded by changes in the frequency of alleles in several generations. This definition, given by evolutionary geneticist
Theodosius G. Dobzhansky , rejected the assumption that genes are the only source of inherited variability and, therefore, the only material with which natural selection can work for the emergence of phenotypic changes in several generations. However, it is worth remembering that Charles Darwin was blissfully unaware of the differences between genetic and non-genetic variability. Darwin's outstanding idea was that natural selection applied to hereditary variability within a population could cause changes in the average characteristics of organisms in several generations, because those inherited properties consistently associated with a large number of surviving descendants would be represented in a larger proportion of individuals in every generation. [Darwin, CR On the Origin of Species (1859)] The inclusion of non-genetic mechanisms in heredity does not require changes in the basic Darwin equation.
One of the categories of non-genetic effects — the
maternal effect — is so obvious that its existence has been recognized for several decades. By definition, the maternal effect occurs when the maternal phenotype affects the descendant phenotype, and this effect cannot be explained by the transmission of maternal alleles. [Wolf, JB & Wade, MJ. What are the maternal effects (and what are they not)? Philosophical Transactions of the Royal Society B 364, 1107-1115 (2009); Badyaev, AV & Uller, T. Parental effects in ecology and evolution: mechanisms, processes, and implications. Philosophical Transactions of the Royal Society B 364, 1169-1177 (2009)] Such an effect can benefit from many methods of influence on the descendants of mothers, including
intergenerational epigenetic inheritance , variability in the structure of the egg, the intrauterine environment, the choice of mother for egg laying. or the birth of children, environmental changes that the offspring will face, postpartum psychological and behavioral interactions. Some maternal effects are a passive consequence of the characteristics of the mother associated with the development of children (including the harmful effects of maternal poisoning, illness or aging), while others represent reproductive investment strategies that have developed to improve the success of reproduction. [Badyaev, AV & Uller, T. Parental effects in ecology and evolution: mechanisms, processes, and implications. Philosophical Transactions of the Royal Society B 364, 1169-1177 (2009); Marshall, DJ & Uller, T. When is a maternal effect adaptive? Oikos 116, 1957-1963 (2007)] Such effects may improve or worsen the physical form of mothers and their offspring.
Until recently (the 1990s), maternal effects were treated no more than minor troubles — the source of the “mistakes” of genetic research related to the environment. But genetics, at least, were convinced that in most species (including key laboratory “
model organisms ”, for example, flies and mice), fathers can only transmit genetic alleles to their children. However, recent studies have discovered many examples of paternal effects in mice, fruit flies, and many other species. [Crean, AJ & Bonduriansky, R. What is a paternal effect? Trends in Ecology & Evolution 29, 554-559 (2014)] In species that reproduce sexually, paternal effects can be just as common as maternal effects.
The environment and experience, age, and genotype of both parents can influence offspring. An environmental factor, such as a toxin or nutrient, can lead to changes in the parent’s body, affecting the development of the offspring. As we shall see, the deterioration of the state of the body due to aging can also affect the reproductive properties and inherited non-genetic factors, and, consequently, the development of offspring.
Cases in which the expression of parental genes influences the phenotype of a child are known as “indirect genetic effects” [Wolf, JB, Brodie, ED, Cheverud, JM, Moore, AJ, & Wade, MJ Evolutionary Rally]. Trends in Ecology & Evolution 13, 64-69 (1998)]. Contradicting intuitions, such effects fit into the concept of non-genetic inheritance, since they are controlled by the transmission of non-genetic factors. For example, a certain gene that has committed expression in a parent may affect its behavior towards the child or change the epigenetic profile of other genes in the
germ line , thus affecting the development of the offspring, even if they do not inherit this gene.
A striking example of indirect genetic influence was found in the study of mice. Vicky Nelson and colleagues crossed bred-bred breeds of mice to get males that are almost identical to each other genetically, with the exception of the
Y chromosome . Then they asked a strange question: does the male Y chromosome affect the daughters phenotype? Anyone who has not slept in biology lectures knows that daughters do not inherit the Y chromosome of their father, therefore, according to the logic of classical genetics, the genes of the parent Y chromosome cannot influence daughters. However, Nelson and his colleagues found that the individual characteristics of the Y chromosome influenced the different physiological and behavioral properties of daughters. Moreover, the influence of the parent Y chromosome on daughters was comparable in strength to the influence of the parent
autosome , or X chromosome, which the daughters inherit. And although the mechanism that worked during this process remains unknown, the Y chromosome genes somehow had to change the sperm cytoplasm, the sperm epigenome or the seminal fluid composition, which allowed the Y chromosome genes to influence the development of the progeny that did not inherit these genes [Nelson, VR, The Spiezio, SH & Nadeau, JH Transgenerational Effects of the Chalosome on daughters' phenotypes. Epigenomics 2, 513-521 (2010)].
Some maternal and paternal effects seem to have evolved in order to give offspring a head start in the habitat that they are likely to encounter [Marshall, DJ & Uller, T. When is a maternal effect adaptive? Oikos 116, 1957-1963 (2007)]. A classic example of such a “precautionary” parental effect is the presence of protective properties in the offspring of parents facing predators.
Daphnias are tiny freshwater crustaceans, swimming slowly and pulling away, using a pair of long appendages as oars. They serve as easy prey for predatory insects, crustaceans and fish. Encountering the chemical signs of predators, some daphnids grow thorns on their heads and tails, making them harder to grab or swallow. In such a daphnia, the offspring grows thorns, even in the absence of signs of predator presence, and also changes the growth rate and life history in a way that reduces vulnerability to predators. This intergenerational induction of predator protection is also found in many plants; when they are attacked by herbivores, such as caterpillars, the plants produce seeds that produce unpleasant protective chemicals (or are prone to accelerated release of such substances in response to signs of predators), and similar induced protection may persist over several generations [Agrawal, AA, Laforsch, C., & Tollrian, R. Transgenerational induction of defences in animals and plants. Nature 401, 60-63 (1999); Holeski, LM, Jander, G. & Agrawal, AA Trans-generational defense induction and epigenetic inheritance in plants. Trends in Ecology & Evolution 27, 618-626 (2012); Tolrian, R. Predator-induced morphological defences: daphnia pulex. Ecology 76, 1691-1705 (1995)].
Although it is unclear how parents of Daphnia induce the development of thorns in their offspring, some examples of apparently adaptive maternal and paternal effects include the transfer of certain substances to the offspring. For example, the moths
Utetheisa ornatrix get
pyrrolizidine alkaloids , eating legumes that synthesize this toxin. Females are attracted to the smell of males with large reserves of this chemical, and such males transfer part of the stored toxin as a “wedding gift” through seminal fluid. Females include these alkaloids in the eggs, making their offspring tasteless for predators [Dussourd, DE, et al. Biparental defensive endowment of eggs with plant alkaloid in the moth of Utetheisa ornatrix. Proceedings of the National Academy of Sciences 85, 5992-5996 (1988); Smedley, SR & Eisener, T. Sodium: Moths gift to its offspring. Proceedings of the National Academy of Sciences 93, 809-813 (1996)].
Also, parents can prepare their offspring for social conditions and lifestyle, which they are likely to meet - this is illustrated by the
desert locust . These insects can switch between two surprisingly different phenotypes: a gray-green loner and a black-yellow schooling locust. Locust swarms are characterized by reduced fecundity, shortened life, large brains and a tendency to be knocked down into huge migratory swarms, capable of destroying plants in large areas. Locusts quickly switch from solitary to collective behavior, encountering a large accumulation of insects, and the population density in which females find themselves prior to mating determines the option that their descendants prefer. It is interesting that the full set of phenotypic changes accumulates over several generations, which indicates the cumulative nature of the maternal effect. Apparently, substances that are transmitted to the offspring through the cytoplasm of eggs and the secretion of glands enveloping the eggs affect it, although epigenetic modification of the germline may also play a role [Ernst, UR, et al. Epigenetics and locust life phase transitions. Journal of Experimental Biology 218, 88-99 (2015); Miller, GA, Islam, MS, Claridge, TDW, Dodgson, T., & Simpson, SJ Swarm: Isolation and NMR analysis of the primary maternal gregarizing agent. Journal of Experimental Biology 211, 370-376 (2008); Ott, SR & Rogers, SM Gregarious desert locusts have significantly more compared with the solitarious phase. Proceedings of the Royal Society B 277, 3087-3096 (2010); The Simpson, SJ & Miller, GA. Journal of Insect Physiology 53, 869-876 (2007); Tanaka, S. & Maeno, K. A review of the maternal characteristics of the desert locust. Journal of Insect Physiology 56, 911-918 (2010)].
However, the experience of parents does not necessarily prepare offspring to improve efficiency. For example, parents could incorrectly recognize the signals of their environment, or their environment could change too quickly - and this means that sometimes parents will correct the properties of the offspring in the wrong direction. For example, if Daphnia mothers induce the development of thorns in their offspring, and predators do not appear, the offspring will pay for the development and wearing of thorns, but will not reap any benefits of this feature. In such cases, the warning parental effect can harm the offspring. [Uller, T., Nakagawa, S., & English, S. Weak evidence for anticipatory effects. Journal of Evolutionary Biology 26, 2161-2170 (2013)]. In general, offspring have the difficult problem of integrating environmental signals received by parents with signals obtained directly from their environment — and the best development strategy will depend on which set of signals will be more useful and reliable [Leimar, O. & McNamara, Transitional evolution of transgenerational environments. The American Naturalist 185, E55-69 (2015)].
The warning effect may not work properly, but in general, natural selection should encourage such attempts. However, many parental effects are completely unrelated to adaptation. Stress can have a harmful effect not only on individuals, but also on their descendants. For example, a study by the University of Illinois showed that stickle females subjected to predator attack imitations gave birth to offspring that studied more slowly could not behave appropriately when meeting predators, and therefore the probability of being eaten was higher [McGhee , KE & Bell, AMPHD: Epigenetics and fitness enhancing effects on offspring anxiety. Proceedings of the Royal Society B 281, E20141146 (2014); McGhee, KE, Pintor, LM, Suhr, EL, & Bell, AM Functional Ecology 26, 932-940 (2012)]. These effects are reminiscent of the ill effects of smoking mothers during pregnancy in our species. Studying correlations in groups of people (and experiments on rodents) showed that instead of precautionally developing resistance to respiratory problems in the embryo, mother’s smoking changes the endometrial space so that the child has problems with lungs and a predisposition to asthma and psychological problems, decreases weight at birth, and other difficulties appear [a]. American Journal of Respiratory and Critical Care Medicine 189, 401-407 (2014); Knopik, VS, Maccani, MA, Francazio, S., & McGeary, JE Development and Psychopathy 24, 1377-1390 (2012); Leslie, FM Multigenerational epigenetic effects of nicotine on lung function. BMC Medicine 11 (2013). Retrieved from DOI: 10.1186 / 1741-7015-11-27; Moylan, S., et al. The Norwegian Mother and Child Cohort study. BMC Medicine 13 (2015). Retrieved from DOI: 10.1186 / s12916-014-0257-4].
Similarly, in different organisms, from yeast to humans, old parents often give birth to sick or quickly dying offspring.
Although the transmission of genetic mutations across the germline may contribute to these “effects of the age of the parents”, non-genetic inheritance seems to play a major role here. Therefore, although some types of parental effects represent evolutionary mechanisms that can improve the fitness of individuals, it is clear that some parental effects transmit pathologies or stress. Such effects, which are not related to adaptability, are comparable to harmful genetic mutations, although they differ from them in that they occur under certain conditions.The fact that parental effects can sometimes be harmful suggests that the descendants should have a way to level this harm, possibly blocking certain types of non-genetic information received from parents. This can occur even if the interests of the fitness of parents and children coincide, since the transmission of incorrect signals of the environment or parental pathologies will adversely affect both parents and children. However, as some scholars have noted, the interests of the fitness of parents and children rarely completely coincide, and therefore parental effects can sometimes become the scene of parent-child conflict [Marshall, DJ & Uller, T. When is a maternal effect adaptive? Oikos 116, 1957-1963 (2007); Uller, T. & Pen. I. Under the parent-offspring conflict. Evolution 65,2075-2084 (2011); Kuijper, B. & Johnstone, RA Maternal effects and parent-offspring conflict. Evolution 72, 220-233 (2018)].Individuals try to allocate their resources in such a way as to maximize their own fitness. More precisely, natural selection encourages the strategies of the “inclusive fitness” of the individual and his relatives. If the individual thinks he can produce more than one offspring, he is faced with the need to decide how to divide the cake between several descendants. For example, mothers can maximize reproductive success by producing more children, even if, because of this, their contribution to each individual child decreases [Smith, CC & Fretwell, SD]. The American Naturalist 108, 499-506 (1974)]. But since every single child gets more benefits by taking more resources from the mother,Such “selfish” maternal strategies are costly for children who can develop reciprocal strategies for extracting more resources from their mothers.To complicate matters even more, it is necessary to take into account that the interests of the mother and the father may also differ. As pointed out by David Haig, fathers can often benefit by helping their offspring extract additional resources from mothers, even if this process impairs the fitness of the mother. This is because when males have the opportunity to breed with several females, each of which can also mate with other males, the best strategy of the male will be to selfishly use the resources of each of the partners for the benefit of their own offspring. Such conflicts between parents and children and mothers and fathers for the contribution of parental resources are a potentially important but little-studied area of the evolution of non-genetic inheritance., , , . , . neriidae Telostylinus angusticollis, . : 2 . , , , , , ; , , , , , , .
« » , Telostylinus angusticollis, , . , .- , , ? , , , – .
As a result, large and small brothers appeared, which we then mated with females fed with exactly the same food. By measuring offspring, we found that larger males produced larger offspring than their smaller brothers, and subsequent studies showed that this non-genetic parental effect was probably controlled by substances transmitted in the seminal fluid [Bonduriansky, R. & Head, M. Phenotype in Telostylinus angusticollis (Diptera: Neriidae). Journal of Evolutionary Biology 20, 2379-2388 (2007); Crean, AJ Kopps, AM, & Bonduriansky, R. Revisiting telegony: Offspring. Ecology Letters 17, 1545-1552 (2014)]. However, since the transmitted T. angusticollis ejaculate is tiny in size,orders of magnitude less than a typical ejaculate containing nutrients that the males of some insects transmit, in this case, apparently, nutrients are not transferred from the males to the females or to their offspring.We recently discovered that similar effects can occur in offspring conceived by other males [Crean, AJ Kopps, AM, & Bonduriansky, R. Revisiting telegony: Ecology Letters 17, 1545-1552 (2014)]. Angela Crin received large and small males in the same way as described earlier, and then mated each of the females with both types of males. The first mating took place when the eggs of the female were underdeveloped, and the second two weeks later, after the eggs had developed and received an impenetrable membrane. Soon after the second mating, the females laid their eggs, and the offspring were collected to study the genotype and determine paternity. Since the eggs of the flies can only be fertilized in a mature state (when the sperm enters through a special hole in the shell)and females rarely keep sperm for two weeks, we were not surprised when almost all offspring were children of males mating with females in the second approach., , , . , , , , , . , , , (, , - ), , . (
"
") were widely discussed in the scientific literature before the advent of Mendelian genetics , but their early evidence was completely inconclusive. Our work provides the first modern confirmation of the possibility of the presence of such effects [Dosophila, see: Garcia-Gonzalez, F. & Dowling, Biological Letters 11 (2015)]. Although telegony goes beyond the limits of heredity in the usual sense of "vertical" (parents -children) transfer properties, it vividly illustrates the potential of non-genetic on research that violates the assumption of Mendel.There is ample evidence that in mammals the diet of the parents affects the development of children. Experimental studies of the effects of diet in rats — especially limiting the supply of key nutrients, such as protein — began in the first half of the 20th century in order to study the health consequences of malnutrition. In the 1960s, researchers found with interest that female rats, who were on a low-protein diet during pregnancy, produced children and grandchildren who were painful, skinny, had a relatively small brain with a reduced number of neurons, did not perform well in tests on intelligence and memory. In recent years, researchers, using mice and rats as experimental models, have turned to attempts to understand the effects of excessive or unbalanced diets,trying to understand the epidemic of obesity among people, and it has already been established that both the mother’s diet and the father’s diet can influence the development and health of children in various ways. Some of these effects occur through the epigenetic reprogramming of embryonic stem cells in the womb. For example, in rats, a high-fat mothers diet reduces the amounthematopoietic stem cells (hemocytoblasts) generating blood cells, and a diet enriched with methyl-supplying drugs increases the number of neural stem cells in the embryo [Kamimae-Lanning, AN, et al. Maternal high-fat diet and obesity compromise fetal hematopoiesis. Molecular Metabolism 4, 25-38 (2015); Amarger, V., et al. The cell line in the body of the rat hippocampus. Nutrients 6, 4200-4217 (2014)]. In rats, a high-fat diet reduces insulin production and glucose tolerance in their daughters [Ng, SF, et al. Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 467, 963-966 (2010)]. Obtained evidence of similar effects in humans.If you try to assess the current state of knowledge in the field of extended heredity, the state of genetics in the 1920s or molecular biology in the 1950s comes to mind. We know enough to appreciate the depth of our ignorance, and to recognize the difficulties ahead. But one thing is already clear for sure - Galtonthe assumptions that have formed empirical and theoretical studies for almost a hundred years are violated in many contexts, which means that biologists are going to have interesting times. Empirical researchers will spend many years studying the mechanisms of non-genetic inheritance, observing their environmental impact, and establishing their evolutionary consequences. This work will require the development of new tools and planning ingenious experiments. The theorists will have the same important task of refining ideas and issuing predictions. At the practical level, for medicine and public health, it is now clear that we don’t have to be “passive transmitters of the nature we received,” since our life experience plays a nontrivial role in shaping the hereditary “nature” that we pass on to our children.– . – . « : » (Extended Heredity: A New Understanding of Inheritance and Evolution by Russell Bonduriansky and Troy Day)