GENETIC PRIMING; HOW ADAPTIVE BEHAVIOUR SHAPES THE GENOME

ABSTRACT

With regard to Organic Selection, it is suggested that the prevalent step-by-step, incremental hypothesis is logically possible but unlikely to account for much of the adaptive behaviour that we witness in nature. An alternative, hypothetical process - Genetic Priming – is described that is considered more likely. It proposes that there is no assimilation of the behaviour into the species genome at all. It suggests that, over the course of many generations, the relevant genes change to variants that support/ encourage the particular adaptive behaviour. Just a simple environmental trigger is then required for the behaviour to be produced. A number of studies are cited and outlined that have given results that appear to be inconsistent with the incremental hypothesis but consistent with the Genetic Priming hypothesis.

ADDITIONAL KEYWORDS: Species genome – organic selection – gene variants – alleles – assimilation – environmental trigger – incremental hypothesis – religiosity.

INTRODUCTION

The modern version of Organic Selection suggests that the evolutionary trajectory of living organisms is not totally dependent on random genetic mutation. It hypothesizes that to some extent and in some way organisms, unconsciously of course, participate in guiding their own evolution. The – rather patchy – history of scientific interest and theoretical/research activity in this area has been set out elsewhere and will not be duplicated here (see e.g., Weber & Depew, 2003; Corning, 2013). In this short paper, I want to suggest that a persistent adaptive behaviour can indeed impact the species genome, and I describe a mechanism – which I call Genetic Priming – that would enable this to occur.

Of course, this is not to suggest that behaviour is the sole driver of Organic Selection. It is well established that a change to the environment can generate a response via phenotypic plasticity. The various molecular processes involved – DNA methylation, histone acetylation etc – have recently been well described and substantiated in Carey (2012). There is substantial evidence that these epigenetic modulations to the genome are often heritable (see in particular Waddington, 1953, 1957; Jablonka & Lamb, 2005). Of course, an environmental change will often be accompanied by a change in behaviour. Where this occurs, I suggest that these epigenetic modulations run alongside and may even interact with the Genetic Priming process.

            The suggestion that behaviour can, in due course, be assimilated into the genome – later called ‘The Baldwin Effect’ by Simpson (1953) – had been proposed by the original Organic Selectionists such as Baldwin, Morgan and Osborn at the end of the 19^th Century. Their suggestions for the mechanism in operation were understandably fuzzy; Mendel’s laws were only just being rediscovered at that time and the discovery of genes/genomes was yet to come. More recent work (e.g. Bateson, 2004; Jablonka & Lamb, 2005), has described a step-by-step incremental assimilation of adaptive behaviour into the genome. Bateson (2004: 289) describes the following scenario with regard to the Galapagos woodpecker finch that pokes sharp sticks into holes to get at insect larvae.

            “In the first stage, a naïve variant of the ancestral finch, when in foraging mode, was more inclined to pick up sharp sticks than other birds. This habit spread in the population by Darwinian evolution because those behaving in this fashion obtained food more quickly. At this stage, the birds still learn the second part of the sequence. The second step is that a naïve new variant, when in foraging mode, was more inclined to poke sharp sticks into holes. Again this second habit spread in the population by Darwinian evolution. The end result is a finch that uses a tool without having to learn how to do so.”

            But much adaptive behaviour does not lend itself to a step-by-step incremental process of this kind. Is it likely that the rooting reflex of the primate neonate was assimilated into the primate genome in this way? Also, at each stage in the process, the new partial implementation must be more adaptive than the last one. Is a finch that carries a sharp stick but doesn’t know what to do with it yet at a fitness advantage to a finch that doesn’t have the stick-carrying fetish? I think not; it would obviously be a hindrance. Finally, the process as described would result in a full assimilation into the genome. However, there is empirical evidence that suggests that an environmental trigger is often necessary. I will present examples of this evidence later in this paper. I suggest that the incremental assimilation procedure is logically possible but unlikely to account for much of the adaptive behaviour that we witness in nature.

            In West-Eberhard (2003), the author takes an alternative approach to describing the impact of organic selection on the relevant genome. She writes: “Generations of organic selection can lead to genetic (congenital or phylogenetic) change that makes the accommodation the norm in the population. Note that this does not imply that the advantageous response becomes genetically determined or genetically assimilated, only that the ability to produce the response becomes more common or fixed due to genetic change.” The Genetic Priming hypothesis that I will now outline goes on to suggest the inter-generational positive feedback mechanism between adaptive behaviour and positively associated gene-variants (alleles) that causes this to occur, and that an environmental ‘trigger’ will always be necessary for the adaptive response to be manifested.

GENETIC PRIMING

The Genetic Priming hypothesis is an alternative suggestion to explain how an adaptive behaviour shapes the genome. In common with West-Eberhard (2003), it proposes that there is no assimilation of the behaviour at all; merely that, over the course of many generations, the relevant genes change to variants that support or encourage the particular adaptive behaviour.

The hypothesis can be summarised as follows:

Living organisms have, over evolutionary time, acquired genetically-mediated predispositions (in terms of allele-sets) that promote/ encourage behaviours that have proven to be adaptive for their species. These genetically primed behaviours are then able to be invoked/ manifested by simple environmental triggers.

Within a population of a given species, suppose that an adaptive behaviour (AB) is performed for the first time by a particular individual in generation (g), and that this individual consistently manifests AB thereafter, whenever it is appropriate to do so. Suppose also that certain genetically mediated predispositions affect the likelihood that AB will be manifest, and that this particular individual is well-endowed with these predispositions by having alleles that facilitate the expression of AB. Let us imagine that the predispositions are Intelligence and Creativity, for example. The adaptive behaviour may well result in relatively more offspring in generation (g + 1) and a tendency for these individuals to have high values for the positively associated predispositions; with a corresponding high likelihood that AB will be performed by greater numbers in generation (g + 1). This may well be magnified by culturally mediated learning/copying behaviour between parent and offspring. Over evolutionary time, AB will spread through the population by this inter-generational positive feedback between AB and the positively associated predispositions. Selection pressure may well result in the behaviour becoming ubiquitous and occurring earlier and earlier in individual life-cycles. However, AB will never become innate. The predisposition for the behaviour among the population will become widespread and stronger, but an environmental trigger will always be necessary for the behaviour to be manifest.

            To take a specific example; the human tendency toward religiosity appears to be genetically mediated. This is supported by fairly recent empirical studies with young children by Keleman (2004), and also by Barrett (2012). Several twin-studies have also found a significant genetic component in religiosity (e.g. Vance et al., 2010). I suggest that Genetic Priming is the mechanism that has, over evolutionary time, turned the strong potential for religious behaviour into an innate human trait.

Presumably, at some point in our evolutionary past, an individual started to perform the first proto-religious act. Let us imagine that, every morning, he prayed to the god-of-the-mountain. His behaviour may well have enhanced his status in the group and therefore increased his relative fitness via sexual selection and, possibly, the protection of him and his children by group members. In order for the process that I have described above to operate we need to make the (reasonable) assumption that such behaviour would have been positively associated with genetically-mediated predispositions.

Theoretical work in the psychology of religion presented by Atran (2003) and Boyer (2001) reveals three strong contender predispositions. They and other authors have suggested that innate belief in a god is a by-product of the following genetically-mediated predispositions: child/parent attachment, assumed parental authority by children, and the teleological assumption. An example of the last is the adaptive assumption that any unexpected noise from nearby bushes may well be a predator. A false-positive will cost the energy required to run away, but a false-negative will give the predator an easy meal. Our present innate religiosity needs a simple trigger to become manifest. In modern western societies, for example, the reassurance to a bereft small child from a main-carer that their pet is “playing happily in heaven” may be sufficient to provide such a trigger.

            If the Genetic Priming hypothesis is correct, there will always be a number of adaptive behaviours ‘trying’ to prime the genome at any one time. Some will involve predisposition gene-sets that overlap and the various behaviours may well ‘want’ to prime the same genes toward different variants. No adaptive behaviour will ever get its optimal set of alleles; compromise and sub-optimisation for any particular adaptive behaviour are inevitable.

            As an adaptive behaviour spreads in the population it becomes, in effect, part of the environment to which the genome is adapting. New mutations as well as existing allele configurations that support/ encourage the behaviour will bring about positive selective pressure. This is simply Natural Selection at work. Several recent authors have highlighted the importance of particular adaptive behaviours to human evolution – for example Wrangham (2009) on the impact of fire and cooking, Wells (2010) on the impact of farming and animal domestication, and Taylor (2010) on the impact of technology. Once an adaptive behaviour starts to become ubiquitous, Genetic Priming and Natural Selection will often work in concert, concurrently.

            Many evolutionary biologists have suggested that post-weaning lactose tolerance developed in humans in temperate regions where cattle were farmed. In this case the adaptive behaviour was successful milk consumption (Vitamin D enables absorption of calcium; particularly important in temperate regions), dependent on the associated subset of the genome involved in controlling lactose tolerance. The positive feedback process explained above has resulted, in these regions, in the ubiquitous priming of the human genome toward post-weaning lactose tolerance – but not in a genetically assimilated tendency to consume milk! There has been no assimilation of the adaptive behaviour; only Genetic Priming of the associated subset of the genome to facilitate it. This is clearly a case of Organic Selection since the behaviour has impacted the species genome. However, the ubiquity of the behaviour has been environmentally constrained because not all geographical regions are suitable for cattle husbandry.

SOME RELEVANT EMPIRICAL STUDIES

Watson & Rayner (1920) demonstrated that we are born with the ability to feel fear. Although a baby will show fear of a loud noise, it will not show fear of a close naked flame until it is brought close enough to be uncomfortably hot. A baby is able to feel the 'fear emotion' but fear will only be manifested once the danger source is physically experienced. Anticipation of danger will only manifest fear once the danger has been associated with the trigger of an unpleasant physical outcome.

The experiments performed on infants by Watson & Rayner would now be considered unethical, and could not be repeated. A relevant and confirmatory study was carried out by Hunt & Smith (1967) on the pecking behaviour of newly-born chicks. They found that the chicks would only peck at "shiny, high contrast targets". In particular, they would peck at their own toes until, by chance, they hit upon food or water. This 'environmental experience/trigger' was found to be necessary before they pecked only at food or water and not their own toes. If their toes were initially masked, and no other shiny targets were available, they didn't peck at all. They appeared to be genetically primed to peck at shiny objects but needed an environmental trigger to peck only at food or water.

            LoBue et al. (2010) found that human neonates exhibited no fear of spiders. However, when tested again two years later, there was pronounced fear. Since the children tested had experienced no harm from spiders in the interim, the authors concluded that the fear had probably been triggered by seeing parental/sibling fearful reactions to the concept and/or presence of spiders.

            Marler & Sherman (1985) identified innate differences in the singing behaviour of male swamp and song sparrows by rearing males from the egg in the laboratory, in complete isolation from adult conspecific song. Isolation-reared males of both species displayed several abnormal song features including reduced numbers of notes per song, longer durations of notes and inter-note intervals, and fewer notes per syllable. Despite these and other abnormalities, many species differences emerged that matched differences in the natural singing behaviour of the two species. Subsequently, songs only became normal for their species when the singing of normally reared adult conspecifics was experienced by the birds.

It could be suggested that the abnormal songs of isolation-reared birds may be a partial assimilation of the behaviour into the genome. However, I propose an alternative explanation. The abnormal songs suggest a rough 'sketch' of the complete songs of normally reared birds rather than the assimilation of a discrete part of the songs. The abnormal songs described by the authors would be as expected from the spontaneous behaviour of birds with the same physical vocal equipment as normally-reared birds, but without the experience of hearing the 'trigger'; the musical detail of the normal song for the species. I suggest that the results reported are consistent with the Genetic Priming hypothesis.

Until recently, Anorexia Nervosa was considered to be a purely psycho-social behavioural disorder. However, more recent work has provided evidence that both genes and environment are implicated in the pathology of the disease. It has been found that particular gene/epigenetic variants render individuals more susceptible. For these people, environmental/experiential conditions such as strict dieting and/or depression are liable to trigger the onset of Anorexia Nervosa (Woerwag-Mehta & Treasure, 2008). Some researchers in this area (e.g. Guisinger, 2003) have suggested that the underlying predispositions referred to may have been adaptive deep in our evolutionary past. Guisinger in particular suggests that they may have enabled survival when famine threatened. This gene/ environmental account of the aetiology of Anorexia Nervosa is also consistent with the Genetic Priming hypothesis, as it appears that a once adaptive – now potentially pathological – predisposition can be triggered by particular present-day environmental/ experiential factors.

            In each of these research programmes, the adaptive behaviour in question appeared to need an environmental trigger to be manifested. The behaviour was not produced – in whole or part – in the absence of such a trigger. This would seem to indicate that the behaviour had not been assimilated into the genome. These results are inconsistent with the step-by-step incremental mechanism mentioned in the Introduction because such a process would be expected to result in genomic assimilation without the need for an environmental trigger. Therefore this hypothesis should be rejected. On the other hand, the results are consistent with the Genetic Priming hypothesis.

SUMMARY

Many biologists accept that, over evolutionary time, adaptive behaviour can impact the species genome. In this brief account I suggest that the leading hypothesis to explain the process – I have referred to it as the step-by-step incremental approach – is inadequate. Building on the work of Mary Jane West-Eberhard (summarised by West-Eberhard, 2003), I propose a new hypothesis, Genetic Priming, as a more likely explanation of the mechanism that drives the phenomenon. Genetic Priming suggests that adaptive behaviour is never assimilated by the genome but, instead, the genome is ‘shaped’ to favour gene-variants that facilitate the adaptive behaviour. A simple environmental ‘trigger’ is then necessary for the behaviour to be expressed. A number of empirical studies are cited that are consistent with this hypothesis.

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