Epigenetic Factors as 'Creative' influence in Evolution

Maybe it’s an issue with loose terminology in my main field of study. Most of the work that I have run into (which is admittedly heavily biased towards evolutionary psychology/evolutionary developmental psychology) has defined epigenetic much more broadly. It seems to suggest that an organism can make proactive changes to its environment and that these changes can be heritable to offspring and grandchildren. It suggest that these heritable changes do not require any alteration in the genes of the organism, though genetic alteration may occur over time. Maybe its better to dump the term epigenetic if it has a more specific meaning in microbiology. It wouldn't be the first time EvoPsych has co-opted a term rather loosely.Examples of what I mean are:
Mice ability to pass information about environments they were reared in to offspring and grandchildren regardless of rearing environment for the offspring (heightened fear response from grandchildren of handled rats)A single celled organism grafted with a portion of membrane from a different organism will pass on the grafted portion not what is "genetically" programmed.A species of fruit fly that started laying its eggs in old world apple tree when they were brought over despite no genetic propensity for the type of fruit, the difference in seasonal variance eventually lead to enough of a pre-zygotic barrier that the species diverged genetically as well as behaviorally.Humans changing priority of health markers in mate selection depending on parasite load in the environment.The question I have is: Do these phenomenon have a mostly genetic basis, just representing genetic networks programmed in the species responding to stimuli? Or are they examples of a form of proactive adaptive behavior that goes beyond genes?I think the answer to this question has ramification for what the 'creative' force is in natural selection and evolution.

Hi PR,
I think most of the examples you provide are genetically based. For example, if an environmental cue causes a transcriptional response in an adult (particularly the germline) and this alters chromsome methylation, histone positioning, etc. in a heritable manner, then it is a change in an epigenetic mechanism with a molecular basis (though the DNA sequence remains unchanged). Another important feature of development has to do with maternal effects. Female eggs contain a lot of RNA's, trancription factors etc. that are critical to development once fertilization takes place. Eggs sit around in the female carrying them for a relatively long time before fertilization takes place and are thus influenced by the environment. This may be why for example, Downs syndrome is more common if the mother is over 40.In all genetic experiments looking for "pro-active" or "pre-adaptive" mutation, the conclusion has been that it does not occur. Epigenetic modification is a more recent discovery but still operates under the principle of heritable change and selection on that change i.e. if you mess up parental imprinting, it either leads to miscarriage or disease like Prader-Willi Syndrome.

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A species of fruit fly that started laying its eggs in old world apple tree when they were brought over despite no genetic propensity for the type of fruit, the difference in seasonal variance eventually lead to enough of a pre-zygotic barrier that the species diverged genetically as well as behaviorally.

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It has actually been found that there was a preexisting latitudinal cline in the maggot fly that predisposed it to shift to the new host:"The importance of speciation without the complete
geographical separation of diverging populations (sympatric
speciation) has become increasingly accepted.
One of the textbook examples of recent speciation in
sympatry is the apple maggot fly Rhagoletis pomonella,
in which genetically differentiated host races feed on
either hawthorn or apple. Three recent articles by Feder
and collaborators show that the history of these host
races is more complicated than was previously realized.
Genes that differentiate races of flies that feed on either
apple or hawthorn are located in chromosomal
rearrangements. This variation forms a latitudinal cline
that must have been established long before apples
were available as hosts. Furthermore, there is also new
evidence for the very recent evolution of a derived preference
for volatile chemicals that are typical of apple
fruits among apple-feeding flies. These results show
that adaptation to apple populations has involved both
the sorting of ancestral adaptive variation and the selection
of novel mutations."Jiggins, C. D., & Bridle, J. M. (2004). Speciation in the apple maggot fly: A blend of vintages? Trends in ecology and Evolution 19: 111-114 http://homepages.ed.ac.uk/...lications/JigginsBridle2004.pdf

Hi PR! Welcome to EVCforum. It's great to see a gen-u-ine evo psych researcher join the forum. It'll be a super addition to the usual run-of-the-mill molecular biologists, geneticists and others of that ilk that haunt this place when they should be working. A word of caution: do NOT engage resident poster Syamasu. He's convinced that evo psych represents the short road to perdition, and is ultimately responsible for every societal ill from eugenics, the Holocaust and the rise of national socialism in 1930's Germany to premature male balding... Otherwise, enjoy your stay - this is a great forum.Back on topic. You stated: I assume you're talking about the apple maggot fly (Rhagoletis pomonella), probably one of the most studied examples of sympatric speciation ever (for obvious commercial reasons). The mechanism and evolution of the two host races - one on hawthorn and the other on imported apple trees - is fairly well understood (or at least has reasonable empirical support). The initial host shift is likely to be related to competition and the availability in the immediate vicinity of a new resource (historical records indicate that many early apple trees were planted in proximity to existing populations of hawthorn). In addition, Rhagoletis appears to be highly plastic (i.e., adaptable). Finally, the heritable component the sympatry is likely related to the evolution of host-specific mating preferences - possibly caused by different chemical composition of the food sources. Interestingly, it appears that the different host races will freely inter-breed when in contact, which means we're not looking at distinct species yet. However, there is evidence that the rate of hybridization is getting smaller - a good indicator that we have a case of incipient speciation happening.To make a long story short, I'm not seeing how the differentiation developing between the hawthorn and apple-specific host races of Rhagoletis pomonella is related to epigenetics. It appears pretty straight-forward neodarwinism. There also doesn't appear to be evidence of "pro-active adaptive behavior" here. Could you expand on how this would be differentiated from any other speciation mechanism?refs:Bush GL, 1992, "Host race formation and sympatric speciation in Rhagoletis fruit flies (Diptera: Tephritidae)", Psyche 99:335—357. Bush is about the most cited authority on Rhagoletis, so you've probably run across him before.Dres M, Mallet J, 2002 "Host races in plant-feeding insects and their importance in sympatric speciation", Phil. Trans. R. Soc. Lond. 357:471—492, provides a good overview of the causes and genetics of host shift in phytophagous insects, including 21 case studies. Although primarily an attempt to develop a new definition and valid criteria for determining sympatry, it gives some good background on the issue from a genetic/ecology perspective.Hawthorne DJ, Via S, 2001, "Genetic linkage of ecological specialization and reproductive isolation in pea aphids", Nature 412:904—907. Although not about Rhagoletus, the article shows much more clearly how resource competition provides the initial impetus to host shift leading to creation of distinct host races - again from a neodarwinian standpoint.Looking foward to your reply.(edited to fix formatting)[This message has been edited by Quetzal, 03-04-2004]

Thanks PR, for that thoughtful answer, I have always been interested in whether the environment of the early African savannah drove early hominids to take advantage of the adaptations and processes that led to bipedal locomotion for instance. Now I have a whole new perspective.

Here is another reference studying rates of adaptation and the effects of the environment on the rate of adaptation..note, it is genetic in originGenetics. 2002 Oct;162(2):557-66. Related Articles, LinksFitness evolution and the rise of mutator alleles in experimental Escherichia coli populations.Shaver AC, Dombrowski PG, Sweeney JY, Treis T, Zappala RM, Sniegowski PD.Department of Biology, University of Pennsylvania, Philadelphia 19104, USA.We studied the evolution of high mutation rates and the evolution of fitness in three experimental populations of Escherichia coli adapting to a glucose-limited environment. We identified the mutations responsible for the high mutation rates and show that their rate of substitution in all three populations was too rapid to be accounted for simply by genetic drift. In two of the populations, large gains in fitness relative to the ancestor occurred as the mutator alleles rose to fixation, strongly supporting the conclusion that mutator alleles fixed by hitchhiking with beneficial mutations at other loci. In one population, no significant gain in fitness relative to the ancestor occurred in the population as a whole while the mutator allele rose to fixation, but a substantial and significant gain in fitness occurred in the mutator subpopulation as the mutator neared fixation. The spread of the mutator allele from rarity to fixation took >1000 generations in each population. We show that simultaneous adaptive gains in both the mutator and wild-type subpopulations (clonal interference) retarded the mutator fixation in at least one of the populations. We found little evidence that the evolution of high mutation rates accelerated adaptation in these populations.

I am going to take a step back for a moment and try and link all this into a broader idea. I think the main question I am interested in on this topic is how much control DNA has on morphology and behavior. If DNA is the primary source for both than new behaviors or new morphologies have to await mutation and other alterations to the DNA strand to develop. If on the other hand DNA plays only one part in a much larger picture a whole range of alterations can take place at different levels that create new potential adaptations.I think it’s worth separating the difference between the concept of DNA and the concept of a gene. If you define gene as a heritable unit it can encompass many levels other than just the DNA strand. Such as areas of the molecule that regulate the expression of the strand, the various mechanisms that alter and recode the mRNA in the nucleus, hormone interactions, feedback mechanisms, ect. I think this complex of interactions is the primary source of heritable information, and the actual DNA codes play only a part in the overall picture. This heritable unit can go beyond just the DNA molecules, histone proteins, and transcription factors. It can include hormones, temperature, population dynamics, cultural standards, and feedback mechanisms (like how bones grow into joints).In addition to my Evo-Psych studies I am working on models of pathways of cellular differentiation. The main working model is that different cell types represent different systems of "genes" turning each other on and off. The model assigns either an 'on' state or ‘off’ state to each gene and then randomly assigns various Boolean functions between the genes. For example: If X is on then Y is off. If Y and X is on Z is off. If Z or Y are on X is off. The more genes you have the more hideously complex the Boolean network becomes. Dr. Stuart Kaufmann originally set up these kinds of networks in the 70’s and discovered that there are many states that get locked into repeating cycles so that you may go through 20 different on/off states and then go back to where you started. He hypothesized that these cycles were different cell types. I have been working with Dr. Kaufmann on several models for how a cell moves from one state to another. The next question about these pathways is how do they evolve. The evolution of these pathways is starting to be modeled now (assuming NIH comes through with some money!) but the actual content of the DNA plays only a minor role. The evolvability of these mechanisms requires a very large holistic model of all the interactions of the genes and regulators, and also the systems that create noise in the process along with a host of other factors. There are million pieces to this puzzle that could be altered and have drastic effects. I think this starts to bring up the question that the DNA is USED by the heritable system and is not THE heritable system.In evolutionary psychology there is a core set of basic behavioral and mental faculties that have been brought to humans through the evolutionary chain. Some more recent than others. What you find is that these various basic functions get constantly co-opted and changed and prioritized depending on a whole host of environmental cues. I have already talked about the example of parasite load changing priority of health cues. Status seeking behavior in males is another big one. Culturally what gives one male more status than another is fairly arbitrary and highly variable, males will pursue these status indicators to their near demise no matter what they are. And on top of that they will not even know why they are doing it, they just know they want whatever it is. Money is an example. Most men who pursue money see it was an end in itself not simply as a mate value thing. Increasing relative mate value has a genetic basis far in the past, while pursuit of money is a culturally transmitted. So the proximate cause and the ultimate cause are separate but similar, if the results of the proximate cause last a long time and are selected for I think they can become ultimate causations for behavior in future generations.
I guess more succinctly the idea I am trying to put forth is that an ultimate cause can produce highly variable responses depending on the proximate causations. If these proximate causes create enough variation in responses and some of the responses are better than others the proximate cause can be selected for even though it may lie in cultural or hormonal or cytoplasm events.I think my example of the maggot flies was shown to be a poor example of this behavior so I will go ahead and withdraw it as an example. But let me try describing another example and how it represents why I wonder if DNA is not the CAUSE of a change but is a tool being used in an adaptive behavior.Tiger salamanders have a cannibal morphology that has a low but significant occurrence in nature. Several studies have examined what causes the morphology to come into being. There has to be three environmental influences present, if any one of them is missing the morph never shows up. First there must be a large number of chorus frog larvae present (or other larvae similar to the tiger salamander larvae), second there must be a large number of tiger salamanders in the area and three there must be a shortage of zooplankton the preferred prey for the salamander. If all three of these are present SOME salamander larvae grow into the cannibal morph. The salamanders are genetically as identical as any species is, all receiving the same environmental influences. Obviously this is a very tightly balanced interaction between environmental influences and genetics. The salamander activates a series of developmental genes to create the cannibal morph. Is the propensity to activate these genes a DNA code in and of itself? I am not convinced. The percentage of morphs even in environments that should trigger it is extremely rare. And the ability to develop the morph stays in the populations even after multiple generations with no morphs appearing. Its staying active with out any selection, which makes me think its present in most if not all salamanders. Even given all the right conditions there seems to be some level of choice in development that goes beyond any deterministic process. This third factor could potential be selected for or against, and if heritable could produce changes in the frequency of a behavior with out the need to invoke DNA mutation.That’s the main point I am trying to make here. If the genetic unit is a complex area of cultural, hormonal, regulatory, stochastic, and DNA interactions significant changes to the development, morphology and behavior of an organism could be achieved without a change in the DNA structure. This offers a different force in generating ‘creative’ adaptations in evolution. If a change is made in a regulatory system or regulatory systems for the regulatory systems, ect. You could see much more significant changes in organisms even in only a hand full of generations.

I am not sure the full significance of the Escherichia coli study. It seems to point to a particular area where increased mutation rates could create a beneficial adaptation in species that produces many generations in consistently harsh environment. But species with a much larger generation time and/or more variable environment would still have a tendency to limit mutations. To me this suggests that there is power to be found in adaptive changes that lie outside of DNA changes.

Hi PR,I don't think too many people are going to violently disagree with this part: At least, as far as the effects of environmental triggers on both development - which may or may not be directly linked to adult morphology - and behavior. Behavior especially is highly modifiable by environment. Examples of learned behaviors abound in organisms as disparate as birds and primates (one of my favorite examples is the natural history of the Cocos Island Finch, which is a heterospecific behavioral mimic). I also don't think anyone is going to be arguing with your contention that DNA plays only one part - albeit IMO a fairly major one - in the phenotype (including behavior) of organisms. Adaptation can take numerous forms for numerous causes. However, I would argue that the fundamental genetic basis for either morphology or behavior must be in place in the genotype for any of these modifications to be inheritable. Mutation is simply the major way in which new variations are created in populations of most organisms. Humans, OTOH, seem to be more influenced by culture than biology. As it is clear that "cultural evolution" works at a substantially faster pace than biological, this is unsurprising. However, it isn't clear that the same applies to other organisms.On a side note, I have to apologize in advance for once again questioning one of your examples. There have been a number of studies done on A. tigrinum that indicate a) the development of cannibal morphs is critically dependent on environmental cues (see, for example, Hoffman EA, Pfennig DW, 1999, "Proximate causes of cannibalistic polyphenism in larval tiger salamanders", Ecology 80:1076-1080) and b) the "ability" to switch is genetically determined (see, for example, Pfennig DW, 1990 "The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole" Oecologia 85:101-107 and Pfennig DW, Collins JP, 1993 "Kinship affects morphogenesis in cannibalistic salamanders" Nature 362:836-838). Finally, the idea that the ability to switch is genetically determined is underlined by the fact that morphogenesis into the cannibal morph can be stopped when the environmental cue is removed (see, Reilly SM, Lauder GV, Collins JP, 1992 "Performance consequences of a trophic polymorphism: feeding behavior in typical and cannibal phenotypes of Ambystoma tigrinum" Copeia 1992:672-679). Facultative metamorphosis into the cannibal variant is, as you said, environmentally triggered. However, the ability to do so is coded in the DNA and inherited. Absent the environmental cue, the existing capability is never expressed, and is simply passed on to the next generation with all the rest of the genotype. With the right trigger, we have critters eating their conspecifics.It's entirely possible I'm still missing what you're arguing. Excuse me if that's the case.

I guess I am not convinced that DNA is a controlling mechanism. Certainly the instructions present in the DNA molecule are necessary to for the creation of all the regulatory and structural properties of the organism. But that doesn't mean its the deterministic part of the system. The examples I have given certainly have a genetic basis, exemplify classic genetic/environmental interaction but more than that I don't think you can explain what happens by an appeal to the genes. Genes seem to be activated or not activated by forces that lay outside of the genes.For example, the Boolean network model does not have any "control" genes in that they regulate the various expressions of all the possible regulators. Instead it is a giant spider web of rules, the cell differentiate in this model either through noise or some form of random fluxuations. Therefor, this initial developmental step is in the genes in that certain sets of genes code for certain cell types but the ability to achieve differentiation is not in the genes. The evolvability of the mechanism to me has to lie in the environment that then acts on the genes. The genes are a tool in this sense not managers. I am not sure I actually agree with this. It depends on what you mean by culture or biology. I think every culture while distinct in many arbitrary ways basically falls under the same fundamental model. This model was defined in the human EEA (Environment of Evolutionary Adaptiveness). My point is that the behavioral aspects of humans are an inheritable chunk that can under go selection and have just as much staying power as any DNA based behavior. Other organism probably wouldn't have anything approaching the variability of human behavior but I think you can find simpler examples that begin to foreshadow what you find in primates and specifically humans. I agree exactly. My point is that since the genetic propensity is being based down even in the absence of any possible selection (it is not expressed for multiple generations) probably MOST salamanders have the gene. But even when all the right trigger events are present only a small fraction form the morphology. There does not seem to be any deterministic part in this equation. If it was only gene/environment interaction I would expect to see a much higher percentage of the morph emerging in laboratory conditions.

Hi PR. Thanks for your reply. I don't really disagree with this, except to say that some genes are activated or not activated by non-genetic factors (i.e., environment). However, the folks that take a "genes-eye view" would include the other genes in the body as part of the environment. IOW, whereas the expression of a given gene or genetic cascade may be effected by control genes, they're also often effected by non-control genes or factors. It almost looks like you're trying to analyze what happens to a given gene in isolation from the other genes - even non-control types - and I'm not sure that's valid. I would say that the specific sequences on a strand of DNA that code for the expression of particular genes ARE the fundamental starting points - and that everything else simply modifies how the gene is expressed. Perhaps I'm still not seeing what you're trying to get at (no surprise, genetics is not my field). Umm, okay. I'll grant you the evolvability of the system is dependent on environmental factors - after all, that's what natural selection is all about. However, I think I disagree with your statement that the ability to achieve differentiation is not in the genes. There are several interesting current research hypotheses that tend to indicate otherwise. For example,

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Kirschner M, Gerhart J, 1998 "Evolvability", PNAS 95:8420-8427

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Evolvability is an organism’s capacity to generate heritable phenotypic variation. Metazoan evolution is marked by great morphological and physiological diversification, although the core genetic, cell biological, and developmental processes are largely conserved. Metazoan diversification has entailed the evolution of various regulatory processes controlling the time, place, and conditions of use of the conserved core processes. These regulatory processes, and certain of the core processes, have special properties relevant to evolutionary change. The properties of versatile protein elements, weak linkage, compartmentation, redundancy, and exploratory behavior reduce the interdependence of components and confer robustness and flexibility on processes during embryonic development and in adult physiology. They also confer evolvability on the organism by reducing constraints on change and allowing the accumulation of nonlethal variation. Evolvability may have been generally selected in the course of selection for robust, flexible processes suitable for complex development and physiology and specifically selected in lineages undergoing repeated radiations.

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Another, a bit more extended, treatment is given in Lynn Caporale's popsci book "Darwin in the Genome" (McGraw-Hill, 2002). For a non-specialist like me, this was a thought-provoking book. I agree with this. However, I think I need to clarify what I mean by culture: "Culture or civilization, taken in its wide ethnographic sense, is that complex whole which includes knowledge, belief, art, morals, law, custom, and any other capabilities and habits acquired by man as a member of society" (Edward Tylor, 1920, quoted in Ehrlich P, 2000 "Human Natures", Penguin Science, page 352). Of course, this definition doesn't permit the existence of non-human "cultures", a conclusion I'm not comfortable with. So to refine it a bit, the way I used "culture" refers to those behavioral attributes that are emergent properties of the interactions between members of social species. Change in human-level complex culture is influenced by mechanism(s) analagous to, but not equivalent to, those involved in natural (phenotype) selection. Although, as culture is based on behavior there are inheritable genetic underpinnings, one of the key differences is that culture can be transmitted laterally as well generationally. Culture - or aspects of it anyway - can ALSO be modified (evolve?) in a single generation, unlike behaviors that are more dependent on genetics, which can mostly only evolve over multiple generations. I'm not sure this necessarily follows. The pattern of cannibal morph expression appears close to what I would expect to see if the allele is maintained in the species at relatively low frequency. Not all, or even most, members of the population would necessarily posess the allele. In addition, the environmental triggers are complex - and can include even the increased probability of inducement of cannibal morphs in populations that already contain cannibal morphs compared with populations that don't. IF there's no trigger present, then there would be no reason for the allele to be under selection - and it would then "hitch-hike" down the generations effected by drift or other stochastic processes. I don't know what linkages there are - i.e., whether the gene complex that creates the cannibal morph is linked to some other set of genes that IS under selective constraint and hence conserved in the population. Tis a puzzlement...

By the way, I'm curious about what you want to suggest. A sort of backward system involving the brain in deciding the hormone level of the cell environment and influencing the suppression of particular genetic code? I think you're right in suggesting that the coupling between information in the genetic material and in the environment is tighter than often suggested.You seem to refer to a inheritable system that is parallel to the information (m)DNA transmits (not only to alternative/direct environment influences). That does have something to do with evo psy, I guess?

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Some nizzle-dizzle (not that important): Developmental selection is a part of environmental selection. So, the question is (and only is) 'versa': how would developmental selection NOT reflect environmental selection? Because developmental selection gives rise to a lot of other restrictions, sometimes more loosely. It doesn't predict which organism will survive. Cognition processes are caused by a mixture between genetic and environmental factors? I think the part of genetics is only important in regard to brain development. Do you know a serious study about that?

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Cognition processes are caused by a mixture between genetic and environmental factors? I think the part of genetics is only important in regard to brain development.

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It actually goes beyond brain development. Mice with mutations in the mono amine oxidase gene (MAO) are highly aggressive. There are similar psychiatric disorders in humans associated with this gene regardless of environment i.e. predominantly genetic effect. In addition, small genetically determined changes in gene expression, particularly developmental genes, can have wide repercussions for cognition. Downs syndrome is genetic and has a clear effect on later cognition regardless of environment. However, once the brain is formed, most cognitive determinants will be environmental as you state. But genetics and epigenetics can have a profound effect as well throughout life.

I am convinced the biggest error in modern biological interpretation is the insistence on there being "feedback" etc loops. That is why I am honing my understanding of Einstein's physical intuition. I'll get back to you once I have mastered the physics to the best of the non-biological participants here.

Of course you're right, the result of brain development can lead to cognitive abilities, but the cognitive processes itself aren't caused by genetic factors. That's only building the system (which can be delayed). It's a interesting question how much of the systems are predesigned by evolution. For example, do we possess a 'language organ' (Chomsky)?