Download GENES, ENVIRONMENTS, AND CONCEPTS OF BIOLOGICAL

GENES, ENVIRONMENTS, AND CONCEPTS OF BIOLOGICAL INHERITANCE
Matteo Mameli
King’s College, Cambridge, CB2 1ST, UK; [email protected];
http://www.phil.cam.ac.uk/~gmm32
The term ‘inheritance’ is used is often used to talk about biological traits. It can be argued that
in this context the term is used to express two different concepts. The first concept refers to
the processes responsible for the reliable reoccurrence of biological features within lineages.
The second concept refers to the processes responsible for the reliable reoccurrence of
phenotypic differences between lineages. I will call these two concepts, respectively, ‘the
concept of inheritanceF’ and ‘the concept of inheritanceD’, where ‘F’ stands for ‘features that
reoccur within lineages’ and ‘D’ stands for ‘differences that reoccur between lineages’.
InheritanceF and inheritanceD are the processes to which these two concepts refer.
The distinction between inheritanceF and inheritanceD is of fundamental importance for
understanding the relation between developmental theory and evolutionary theory. Once this
relation is properly grasped, it’s not difficult to realize that the currently popular gene-centric
views of inheritanceF and inheritanceD are inadequate. The received view is that, apart for
those traits that are under the influence of cultural processes, genetic transmission is the only
process responsible both for the reliable reoccurrence of features within lineages and for the
reliable reoccurrence of differences between lineages. That is, inheritanceF and inheritanceD
are due to genetic transmission and to nothing else. In this chapter, I will argue that both the
received view about inheritanceF and the received view about inheritanceD are wrong (Mameli
2004, 2005). I will examine and reject some of the claims Richard Dawkins makes in The
Extended Phenotype. Dawkins explains what the evolutionary version of the gene-centric
view is and is not committed to. His conclusions rest on mistaken assumptions, but the
arguments he presents are useful in order to point out how exactly the view defended here
differs from the accepted orthodoxy.
1. InheritanceF
The concept of inheritanceF refers to the processes responsible for the like-begets-like
phenomenon. The like-begets-like phenomenon is simply the fact that biological organisms –
through reproduction – generate organisms with features that are the same as (or very similar
to) those of the organisms that have generated them. Four-legged organisms (usually and
reliably) beget four-legged organisms; two-eyed organisms (usually and reliably) beget twoeyed organisms; insect-eating organisms (usually and reliably) beget insect-eating organisms;
fast-running organisms (usually and reliably) beget fast-running organisms, etc. The likebegets-like phenomenon is obviously not a logical necessity, but it’s something that humans
have known about for a long time. This means that the concept of inheritanceF has been
around for a long time. Interestingly, this concept was around long before the word
‘inheritance’ started being used to talk about biological traits.
Some of the first biological treatises ever written, such as Aristotle’s On the Generation of
Animals and Hippocrates’s On Generation, explicitly talk about the like-begets-like
phenomenon. Aristotle and Hippocrates had theories about the processes responsible for the
reliable reoccurrence of features within lineages and thereby they had a concept of such
processes. Hence, they had the concept of inheritanceF. But they didn’t use (the equivalent in
their native language of) the term ‘inheritance’ to talk about these processes: they didn’t use
inheritance words to express the concept of inheritanceF.
Terms like ‘inheritance’, ‘inherited’, ‘heritable’, etc. were adopted to talk about biological
phenomena only much later. The first occurrences are to be found in the sixteenth century. At
the beginning it was just a metaphor. Inheritance words had been used for a long time to talk
about the transfer of property, wealth, and titles from a person to his descendants. The idea
was that, just like humans inherit their ancestors’ properties, wealth or titles, all organisms
could be seen as inheriting (some of) their ancestors’ biological features. This can be called
the metaphor of inheritance. This metaphor has now become a dead metaphor. This means
that it was a successful metaphor: everyone adopted it and it has become part of ordinary
language. Why was the metaphor formulated? Why was it successful? The metaphor was
formulated and universally adopted because of what I will call ‘the conception/donation
view’. The conception/donation view is any theory saying that the reliable reoccurrence of
biological traits within lineages is due to the transfer at the moment of conception of some
developmentally special material from parents to offspring. The metaphor of inheritance and
the conception/donation view fit each other extremely well. The parent-to-offspring transfer
of developmentally special material can be metaphorically seen in terms of parents at the
moment of conception ‘giving’ or ‘donating’ their own biological features to their offspring.
That is, the offspring can be seen as ‘receiving’ or ‘inheriting’ some of the parents’ biological
features through the material transfer that occurs at conception.
For someone who holds (implicitly or explicitly) some version of the conception/donation
view, the metaphor of inheritance is a very natural way of thinking about the processes
responsible for the like-begets-like phenomenon. The metaphor of inheritance was formulated
and then universally adopted because the conception/donation view was (and still is) an
extremely popular and entrenched way of thinking about the transgenerational stability of
phenotypic form. Almost every explanation of the like-begets-like phenomenon even
proposed is a version of the conception/donation view. For example, both Aristotle and
Hippocrates subscribed to the conception/donation view. They both believed that parentoffspring similarities were due mainly to the transfer of some developmentally special
material at conception, even though they disagreed about the nature of such special material.
Similarly, both Lamarck and Weismann held versions (even though famously different
versions) of the conception/donation view.
The history of scientific biology from the discovery of cells to Watson and Crick’s discovery
of the double-helical structure of DNA was shaped by biologists’ attempts to make the
conception/donation view more and more precise. When gametes were discovered in the
seventeenth century, most scholars in this area immediately assumed that gametic cells were
the means by which the transfer responsible for the like-begets-like phenomenon occurred.
That is, a gameto-centric version of the conception/donation view was immediately adopted.
When cells’ nuclei were discovered in the nineteenth century, a nucleo-centric version of the
conception/donation view was proposed: the like-begets-like phenomenon was seen as due to
the transfer of some important material contained in the gametic nuclei. When chromosomes
were discovered at the beginning of the twentieth century, the gameto-centric version was
replaced by the chromosome-centric version of the conception/donation view: the special
material that is transferred at conception and that causes the transgenerational reoccurrence of
features was to be found in the gametic chromosomes. Then came the results of Avery et al.
(1944), which convinced many that the special material was actually the DNA contained in
gametic chromosomes: this is the DNA-centric version of the conception/donation view.
After Watson and Crick (1953a, 1953b) discovered the double-helical structure of DNA, the
DNA-centric version of the conception/donation view became almost universally accepted.
The discovery of the structure of DNA was important because it convinced many that
something as simple as DNA could, when transferred from parents to offspring, be
responsible for the like-begets-like phenomenon. The combinatorial structure of DNA and its
semi-conservative mode of replication were seen as the definitive solution to the problem of
explaining the transgenerational stability of phenotypic form. On this view, the like-begetslike phenomenon is due exclusively to DNA transmission, with the only exceptions being
those few traits that are due to cultural transmission and that reliably reoccur generation after
generation because of what some researchers nowadays call ‘cultural inheritance’. In other
words, the traits that reliably reoccur can be divided into two classes: those that reliably
reoccur because of cultural transmission (which are a minority and are present only in humans
and perhaps in a small number of other species) and those that reliably reoccur because of
genetic transmission (which are present in all species). Those phenotypic traits whose
transgenerational stability is supposed to be due exclusively to DNA transmission are often
said to be ‘innate’.
Until very recently, the conception/donation view was challenged only very rarely. Very few
speculated that the like-begets-like phenomenon (for non-cultural traits) might be due at least
in part to things other than the material transfer that occurs at conception. Because of this,
many alternative theoretical possibilities were never thoroughly investigated. The problem is
that the conception/donation view is incompatible with what we have discovered about
phenotypic development. Let F be a particular feature that reliably reoccurs in the organisms
of a given lineage. The reliable reoccurrence of F can be due exclusively to some material
transfer that occurs at conception only if the development of F is somehow ‘determined’ by
the special developmental material transferred at conception. Let M be the special
developmental material that an organism obtains from its parents at the moment of
conception. If M is not sufficient for the development of F, the reliable reoccurrence of M
(due to transfer at conception) cannot be sufficient for the reliable reoccurrence of F. Let us
apply this to the DNA-centric version of the conception/donation view. The reliable
reoccurrence of a feature in a lineage can be due exclusively to the parent-to-offspring
transfer of some DNA sequence only if the DNA sequence is itself sufficient to determine the
development of the feature. If the development of the feature requires both the DNA sequence
and some other factors, the reliable reoccurrence of the DNA sequence cannot be enough for
the reliable reoccurrence of the feature. The other factors must reliably reoccur too. But we
now know that no phenotypic feature of an organism is entirely determined by the DNA
sequences that the organism has obtained from its parents at the moment of conception. All
phenotypic traits result from the interaction between DNA sequences and non-genetic factors
and, more generally, between factors that an organism obtains at conception from its parents
and factors that are not involved in such transfer. Thus, neither the DNA-centric theory of
inheritanceF nor any other version of the conception/donation view can be right.
Nowadays few biologists believe that there is any phenotype for whose developmental
parentally derived DNA is sufficient. But many believe that the developmental interactions
between genetic and non-genetic factors are – at least in the case of innate traits – relatively
simple, and that genetic factors are causally and explanatorily privileged. This assumption is
what drives the use of the many informational metaphors so popular in biology. The genome
is seen as a ‘blueprint’, or a ‘recipe’, or a ‘program’. Innate traits are genetically encoded. The
non-genetic factors involved in the development of these traits are seen as whatever is needed
for the genome to ‘manifest’ or ‘realize’ or ‘express’ itself. Non-genetic factors are seen as
mere ‘mortar and bricks’ (in the genome-as-blueprint conception), or as mere ‘ingredients’ (in
the genome-as-recipe conception), or as mere ‘hardware’ (in the genome-as-program
conception). Non-genetic factors are general-purpose: they don’t provide any specificity to
the developmental process. They only play a supportive role. They are necessary, but their
secondary role justifies their omission from developmental explanations.
The assumptions that motivate the application of informational metaphors to the genome are
unjustified. The developmental interactions between genetic and non-genetic factors are not
accurately represented by such metaphors. The study of the genome and of molecular and
developmental pathways has led to many important discoveries that show the inadequacy of
these metaphors. The genome and all the molecular processes occurring within a living
organism are influenced by non-genetic factors in very subtle and specific ways.1 Which
genes are switched on or off at any particular moment, as well as the way the products of
genetic activity are used and transformed, is determined by the cellular context, which is the
result of the interaction between the genetic and non-genetic factors that have affected the
cell. This is true of all traits, including those traits that are said to be ‘innate’ or ‘biologically
inherited’.2
The currently popular versions of the DNA-centric theory of inheritanceF often concede that
non-genetic factors have a role to play in developmental processes, but they downplay the
role of such factors by classifying them as mere causal background. If it were possible to treat
non-genetic factors as mere causal background in explaining the developmental of
phenotypes, it would also be possible to treat them as mere causal background in explaining
the transgenerational stability of phenotypic form. But the fact that we cannot do the former
means that we cannot do the latter. Consider for example the like-begets-like phenomenon as
it applies to human legs. The species-typical structure of human legs reliably reoccurs in
lineages of human beings. The transfer at conception of certain DNA sequences from parents
to offspring is certainly part of the explanation for the reliable reoccurrence of this phenotype.
But it is only part of the explanation. We know for example that the development of human
legs is affected by the amount of thalidomide that is present in the maternal womb as well as
by the acceleration of gravity. Humans that develop in a thalidomide-rich womb or in a
gravity-free environment develop limbs that are markedly different from the species-typical
ones. Thalidomide and gravity influence genetic activity and its products, and they can
produce specific differences in the development of this phenotypic trait. Thus, a complete
explanation of the like-begets-like phenomenon as it applies to human legs will have to
mention not only the reliable reoccurrence of those DNA sequences that are involved in the
development of normal human legs, but also the fact that human maternal wombs are reliably
(even if not invariably) thalidomide-free and that humans reliably develop in an environment
with an acceleration of gravity of roughly 9.8 m/s2.
The reliable reoccurrence of a phenotype requires the reliable reoccurrence of all the factors
responsible for its development. Some of these factors are genetic, but others are not. Some of
these factors are parentally produced (like DNA sequences transmitted at conception and
maternal wombs) and some are due to other kinds of processes going on in the environment
where the organisms live and develop (as in the case of gravity). The DNA-centric theory of
inheritanceF (i.e. the DNA-centric explanation of the like-begets-like phenomenon) is
incomplete and thereby misleading.3
[Insert Fig.1] [Insert Fig.2]
2. InheritanceD
The concept of inheritanceD refers to the processes responsible for the reliable reoccurrence of
differences between lineages. InheritanceF and inheritanceD are different things. This can be
seen by returning to one of the examples discussed in the previous section. The fact that
humans reliably develop in an environment with an acceleration of gravity of roughly 9.8
m/s2 is part of the explanation for the reliable reoccurrence of human species-typical legs in
lineages of humans. That is, the process responsible for the fact that humans reliably develop
1
Mameli and Papineau (2006); Bateson and Martin (1999); Bateson (1976, 1983, 2001); Oyama et al. (2001);
Lewontin (2000); Gottlieb (1992, 1997, 2003); Meany (2003); van der Weele (1999); Thelen and Smith (1994);
Gilbert (2001, 2003a, 2003b, 2003c); Gilbert and Bolker (2003); Schlichting (2003, 2003); Pigliucci (2001a,
2001b); West-Eberhard (2003); Moore (2001); Wassersug (1999); Hall et al. (2003); Moore (2003).
2
Griffiths and Gray (1994, 1997, 2001); Gray (1992, 2001); Griffiths (2001); Oyama (2000a, 2000b); Fox Keller
(2000, 2002); Godfrey-Smith (1999, 2000a).
3
For further discussion see Mameli (2005). See also Griffiths and Gray (1994, 1997, 2001); Gray (1992, 2001);
Oyama (2000a, 2000b); Jablonka (2001, 2004).
in an environment with an acceleration of gravity of roughly 9.8 m/s2 is part of inheritanceF
for human species-typical legs. But all human beings grow up in an environment where the
acceleration of gravity is roughly 9.8 m/s2. So, gravity cannot be responsible for (significant)
differences between human lineages in the shape or structure of legs. Hence, gravity cannot
be responsible for reliably reoccurring (significant) differences in legs between human
lineages (or even between human lineages and chimpanzee lineages). The process responsible
for the fact that humans reliably develop in an environment with an acceleration of gravity of
roughly 9.8 m/s2 is not part of inheritanceD for human legs.4
Some of the factors that affect or contribute to developmental processes are not
transgenerationally stable. For example, in humans there is no correlation between the
climatic conditions that affect the development of a child in the first three months of life and
the climatic conditions that affect the development of his or her children in the first three
months of life. It’s not the case that people born in summer, for example, tend to have
children born in summer.5 Other developmental factors are transgenerationally stable and
their transgenerational stability contributes to the transgenerational stability of the phenotypic
traits that they affect. But not all transgenerationally stable developmental factors are
responsible for phenotypic variation. As said, gravity is not. The transgenerationally stable
developmental factors that contribute to phenotypic variation often result in
transgenerationally stable phenotypic variation, i.e. they result in transgenerationally stable
differences between lineages. The mechanisms responsible for the transgeneretional stability
of those developmental factors that generate phenotypic variation are thereby mechanisms of
inheritanceD.
The concept of inheritanceD is a population-level concept: the application of this concept is
always relative to the variation in a specific phenotypic trait existing in a particular
population. In this, it is very different from the concept of inheritanceF. It can be argued that
the first documented appearance of the concept of inheritanceD is in Charles Darwin’s The
Origin of Species. A proper understanding of the theory of natural selection requires some
grasp of this concept. Natural selection acts on phenotypic variation, but not all phenotypic
variation can be the target of natural selection: only phenotypic variation that reliably
reoccurs is relevant. The connection between natural selection and inheritanceD is as follows:
natural selection requires reliably reoccurring phenotypic variation; reliably reoccurring
phenotypic variation is due to reliably reoccurring variation in developmental factors; the
reliable reoccurrence of variation in developmental factors is due to mechanisms of
inheritanceD.
The DNA-centric theory of inheritanceD is the theory according to which (with the exception
of cultural variation) all transgenerationally stable phenotypic variation is due to variation in
developmental factors – DNA sequences – that reliably reoccur because of genetic
transmission. From this theory it follows that all transgenerationally stable (and thereby
selectable) phenotypic variation is genetic variation. Consider the point of view of someone
who believes in the DNA-centric theory of inheritanceF. According to this person, DNA
segments are the only (causally or explanatorily important) developmental factors that
reliably reoccur. Thus, it is only natural for this person to think that all reliably reoccurring
(non-cultural) phenotypic variation is due to variation in DNA. Very likely, many believe in
the DNA-centric theory of inheritanceD because they believe in (some informational version
of) the DNA-centric theory of inheritanceF. But the DNA-centric theory of inheritanceF is not
the only route to the DNA-centric theory of inheritanceD. There are evolutionary biologists
who believe the DNA-centric theory of inheritanceF to be wrong, and yet hold a DNA-centric
theory of inheritanceD. How can this be?
4
This has to be understood relative to the existing human lineages. Things may of course change if humans start
colonizing and living on planets where the value for the acceleration of gravity is different from the one we have
on Earth.
5
Things are different in species where the young are born in the same season as the parents.
Let’s look at what Richard Dawkins says in The Extended Phenotype (see especially chapter
2, 5 and 6). Dawkins concedes that all developmental factors are in some sense on a par and
that, for every phenotype, both genetic and non-genetic factors play important developmental
roles. By making this concession, he rejects (at least implicitly) the DNA-centric version of
inheritanceF: if both genetic and non-genetic factors are important in phenotypic
development, the reliable reoccurrence of phenotypes must require the reliable reoccurrence
of both genetic and non-genetic factors. But, Dawkins claims, the evolutionary biologist is not
interested in the transgenerational stability of phenotypic form. Rather, she is interested in the
transgenerational stability of phenotypic differences. She is interested in reliably reoccurring
phenotypic differences because these differences are what natural selection can ‘see’ and ‘act
upon’, and the evolutionary biologist is primarily interested in natural selection. Dawkins is in
effect suggesting that inheritanceF should be of little concern to the evolutionary biologist (as
opposed to the developmental biologist). The evolutionary biologist should focus only on
inheritanceD. And when one focuses on inheritanceD, according to Dawkins, the DNA-centric
theory regains centre stage: even if genetic transmission is not enough for inheritanceF,
genetic transmission is certainly enough for inheritanceD. Apart from cultural differences,
only phenotypic differences due to genetic differences are transgenerationally stable and
thereby only such differences are selectable. The DNA-centric theory of inheritanceF may be
abandoned, but the DNA-centric theory of inheritanceD is correct.
Some of the arguments that Dawkins presents in support of the DNA-centric theory of
inheritanceD have to do with his conception of the replicator and with the idea that only genes
(and perhaps memes, for the cultural case) are replicator-like. These arguments have been
criticised by others and there is no room to examine them here.6 But there is also another
argument that Dawkins uses and that has nothing specifically to do with the special properties
of replicators. According to this argument, all non-genetic factors involved in the
development of non-cultural traits are of two kinds: either they are invariant across lineages
or there is no significant parent-offspring correlation in the way their variation is distributed.
If non-genetic factors are invariant across lineages, then they are unable to produce
phenotypic variation and thereby they cannot be involved in the reliable reoccurrence of
phenotypic variation. If the way non-genetic factors are distributed changes from one
generation to the next, then the phenotypic variation that they produce in one generation
cannot be correlated with the phenotypic variation that they produce in the next generation
(where the correlations are measured in terms of similarities within single lineages) and,
thereby, they cannot give rise to transgenerationally stable phenotypic variation, that is, they
cannot give rise to stable differences between lineages.7 Either way, whether they vary or not,
non-genetic factors are not responsible for reliably reoccurring (non-cultural) phenotypic
variation. Since inheritanceD is concerned exclusively with reliably reoccurring phenotypic
variation, it follows that non-genetic factors play no role in inheritanceD (for non-cultural
traits; from now on I will take it as given that we are talking only about non-cultural traits).
The problem with this argument is that it is based on a false assumption. It’s just not true that
all non-genetic developmental factors either don’t vary at all or vary in ways that are not
transgenerationally correlated. The following thought experiment can help us understand how
this could be the case (Mameli 2004).
6
7
Gray (2001); Godfrey-Smith (2000b); Sterelmy et al. (1996); Sterelny (2001, 2004); Mameli (2004).
Read, for example, the following passage: ‘It is strictly incomplete to speak of blue eyes as the ‘effect’ of a given
gene G1. If we say such a thing, we really imply the potential existence of at least one alternative allele, call it G2,
and at least one alternative phenotype, P2, in this case, say, brown eyes. Implicitly we are making a statement
about a relation between a pair of genes {G1, G2} and a pair of distinguishable phenotypes {P1, P2}, in an
environment which is either constant or varies in a non-systematic way so that its contribution randomizes out.
[…] Such an insistence that phenotypes are not caused by genes, but only phenotypic differences caused by gene
differences […] may seem to weaken the concept of genetic determination to the point where it ceases to be
interesting. This is far from being the case, at least if the subject of our interest is natural selection, because natural
selection too is concerned with differences […].’ (Dawkins 1982/1999, 195-196, emphasis added).
Consider a species of butterflies where the females lay their eggs on the same plant on which
they hatch. The mechanism responsible for this phenomenon is an imprinting mechanism.
The butterflies feed on the plant on which they hatch and imprint on the taste of this plant.
When they have to select a plant for oviposition purposes, the memory of the taste of the plant
on which they hatched is used to find a plant of the same species and to perform the egglaying behaviour on this plant. Let us assume that, at one particular stage in the evolution of
this butterfly species, all the individuals hatch on plants of one single species and, thereby, all
females lay their eggs on the same plant species. Let us also assume that, in this butterfly
species, like in many others, size correlates with fitness: the bigger is a butterfly, the higher
are its chances to survive and reproduce. At the particular moment in the evolution of the
species, there is no genetic variation for size in the butterflies. All genetic variation for size
has been ‘used up’ by previous runs of selection. This, of course, doesn’t mean that all the
butterflies are of the same size. It means instead that all the existing differences in size
between the butterflies are due to differences in the non-genetic factors that affect the
development of the butterflies, while none of these differences in size is due to differences in
butterfly genomes. For example, some butterflies are luckier than others in their search for
nutritious foods and, because of this, they become bigger than the average.
Consider now a specific female butterfly whose imprinting mechanism malfunctions as a
result of a developmental accident. Because of this malfunctioning, this butterfly lays her
eggs on a plant that isn’t the usual one. Given the important role that the plant of hatching
plays in the development of caterpillars, a mistake like this would in general produce negative
effects on the fitness of a butterfly and of her offspring. But, accidentally, this particular
butterfly lays her eggs on a plant of a species that has been recently introduced in the
environment where the butterflies live. This plant turns out to have very positive effects on
butterfly development. For this reason, we can call this butterfly ‘the lucky butterfly’. As a
result of eating the new plant, on average, the offspring of the lucky butterfly end up having
bigger body size than the offspring of the other butterflies. This means that, on average, the
offspring of the lucky butterfly have higher fitness than the offspring of the other butterflies.
Hence, on average, the offspring of the lucky butterfly produce more offspring than the
offspring of the other butterflies.
The daughters of the lucky butterfly have in general a properly functioning imprinting
mechanism, since most of them don’t suffer from developmental accidents like the one
suffered by their mother. Therefore, having hatched on the new plant, most of them lay their
eggs on the new plant. The ‘grandchildren’ of the lucky butterfly eat the new plant. Hence,
they have on average bigger body size (and thereby higher fitness) than other butterflies. On
average, they out-reproduce other butterflies. Moreover, the females imprint on the new plant
and, thereby, they lay their own eggs on the new plant. The cycle is repeated and, thanks to
the imprinting mechanism, it continues to be repeated. Because of this process, the number of
butterflies laying eggs on plants of the new species starts to increase. We can even imagine
that, due to competition for reproductive resources, the more numerous the butterflies that
hatch on the new plant become, the more difficult it is for the butterflies that hatch on the old
plant to reproduce. After many generations, the butterflies hatching on the old plant may
become extinct: all the existing butterflies end up hatching on the new plant and they end up
being (on average) bigger than their ancestors were before the whole process started; that is,
the average size goes up.
There are many things to notice.8 The first is that Dawkins is wrong in assuming that nongenetic developmental factors are either invariant or vary in ways that are not
transgenerationally correlated. Plant of hatching is a non-genetic developmental factor that
affects (among other things) butterfly body size. Due to the way the imprinting mechanism
works, the way variation in plant of hatching is distributed in one generation is correlated
8
For a more detailed discussion see Mameli (2004).
with the way variation in plant of hatching is distributed in the next generation. Differences
between lineages with respect to plant of hatching reliably reoccur one generation after
another. And as a consequence of this, differences in size that are due to differences in plant
of hatching reliably reoccur too.
Another thing to notice is that genetic transmission is not involved in the inheritanceD of size
in the butterflies. Since there is no genetic variation for size, there are no phenotypic
differences in size between butterfly lineages that reoccur because of the reoccurrence of
genetic differences affecting size. Instead, there are differences in size between butterfly
lineages that reliably reoccur because of the reliable reoccurrence of differences in plant of
hatching. The reliable reoccurrence of differences in plant of hatching is due to the imprinting
mechanism. So, in this particular species, the mechanism of inheritanceD for the phenotypic
trait ‘size’ is an imprinting mechanism rather than genetic transmission. This applies to the
butterfly species only during the evolutionary transition described above. Before the
transition (when all the butterflies hatch on the old plant) and after the transition (when all the
butterflies hatch on the new plant), there are no reliably reoccurring differences in size due to
reliably reoccurring differences in plant of hatching (since all the butterflies hatch on the
same plant). Thus, before and after the transition, the imprinting mechanism cannot be a
mechanism of inheritanceD for size. In fact, before and after, in a situation where there are no
genetic differences for size and all the non-genetic differences for size are not reliably
reoccurring, there is no inheritanceD for size at all.
Let us focus on what happens during the transition. Reliably reoccurring phenotypic variation
is selectable, independently of what its developmental origins are. Given that, in the case of
the butterfly species, reliably reoccurring variation in size is variation in fitness, this variation
is not just selectable but also selected. The transition involves a process of natural selection:
the statistical composition of the population (the frequency of different phenotypes, which in
this case determines the average size of the population) changes as a result of differences in
fitness between phenotypes (bigger size, smaller size) that are ‘transmissible’ from one
generation to the next. But, differently from the standard case, the phenotypic differences that
get selected in the case of the butterflies are not due to genetic difference. Rather they are due
to non-genetic differences in plant of hatching.
The process triggered by the lucky butterfly increases the frequency of butterflies with bigger
size (a phenotypic trait) and the frequency of butterflies that hatch on the new plant (a nongenetic developmental factor): there is selection for bigger butterflies which result in selection
for butterflies that hatch on the new plant. In the standard cases studied by evolutionary
biologists, Mother Nature selects for certain transmissible genetic variants by selecting for the
phenotypic variants due to those genetic variants. In the case of the butterflies, Mother Nature
selects for certain transmissible variants in non-genetic developmental factors by selecting for
the phenotypic variants due to those non-genetic variants. The process is the same, except for
the fact that in one case the bottom-level reoccurring developmental variants are genetic and
in the other case they are not.
This thought experiment shows that there is no a priori reason to believe that only genetic
transmission can play the inheritanceD-role with respect to phenotypic variation. Thus, there
is no a priori reason to believe that only genetically-caused phenotypic variation is selectable
and that natural selection is always, at bottom, selection of genetic variants. But it’s not just a
matter of mere possibilities. In Mameli (2004), I argue that imprinting mechanisms generate
the reliable reoccurrence of fitness-relevant phenotypic variation. For example, habitat
imprinting generates reliably reoccurring differences in the habitat where organisms grow and
breed, and such differences in habitat generate reliably reoccurring phenotypic differences
that affect fitness. The same applies to locality imprinting (of the kind that occurs, for
example, in some species of salmon) and to imprinting concerning nest location or nest
material materials. Host imprinting generates reliably reoccurring differences in the kinds of
hosts certain parasitic organisms are associated with and, thereby, it generates reliably
reoccurring phenotypic differences due to differences in hosts. A particular kind of host
imprinting is the foster-parent imprinting that occurs in parasitic birds. These birds imprint on
the physical appearance of the adult birds that are present in the nest they are parasitizing and
use the information so acquired in order to lay their own eggs in the nests of similar birds –
birds of the same species, or subspecies, or even lineage (Avital and Jablonka 2001). Another
example is sexual imprinting. Many birds and mammals imprint on the features of the parent
of the opposite sex. In this way they develop a sexual preference for conspecifics that
resemble their opposite-sex parent and, at the same time, they develop a sexual preference
that resembles the sexual preferences of their same-sex parent. Consider what happens to
female birds in species like these. A female chooses a partner according to her sexual
preferences. When a daughter is born, the daughter comes into contact with a father with
features that match the maternal sexual preferences. The daughter imprints on such features
and develops her own sexual preferences accordingly. Thus, the daughter ends up having
sexual preferences similar to those of her mother. In this way, sexual imprinting can generate
the reliable reoccurrence of differences in sexual preferences and, thereby, the reliable
reoccurrence of those differences in fitness that depend on such preferences.
Imprinting is not the only mechanism able to generate non-genetic inheritanceD. Parentoffspring learning (if reliable enough) can generate the reoccurrence of phenotypic
differences between lineages (Mameli 2007). Another important class of mechanisms is
constituted by those responsible for the stability of symbiotic associations. Symbiotic
associations (both endosymbiotic associations and esosymbiotic associations) are incredibly
common and incredibly important from an ecological and an evolutionary point of view.9 The
transgenerational stability of symbiotic associations generates transgenerational stability in
the phenotypic differences due to the kinds of organisms a lineage is associated with. But the
mechanism responsible for the transgenerational stability of symbiotic associations is often
not genetic transmission (Mameli 2005). In some cases, the association is stable and reliable
due to parental behaviour, as in the case of those insects that inject symbiotic bacteria in their
offspring’s eggs. In other cases, the association is stable and reliable because of the structure
of the environment where the two species of organisms live and interact, as in the case of the
symbiosis between legumes and nitrogen-fixing bacteria.
The existence of these mechanisms shows that the DNA-centric theory of inheritanceD and
the view that only genetic differences can be the target of natural selection are wrong.
3. Interactions
The original native (United States) for the female maggot fly’s egg laying was
hawthorn, a spring-flowering tree or shrub. Domestic apple trees were introduced into
the United States in the seventeenth century. Haws and apple trees occur in the same
locale. The first known infestation of apple trees by apple maggot flies was in the
1860s. There are now two kinds of R. pomonella [the maggot fly], one that mates and
lays its eggs on apples and one that mates and lays its eggs on haws. The life cycles
of the two variants are now desynchronized because apples mature earlier than haws.
Incipient speciation has been maintained by a transgenerational behavior induced by
early exposure learning: an olfactory acceptance of apples for courting, mating, and
ovipositioning based on the host in which the fly developed (reviews in Prokopy and
Bush 1993; Bush and Smith 1998). We can only speculate on the cause of the original
shift from hawthorns to apples as the host species for laying eggs. Perhaps the
hawthorn hosts became overburdened with infestations or, for other reasons, died out
in a part of their range, bringing about a shift to apples in a small section of the
ancestral hawthorns population that did not have such well-developed olfactory
9
Margulis (1998); Margulis and Fester (1991); Margulis and Sagan (2002); Douglas (1994); Paracer and Vernon
(2000); Wakeford (2001); Maynard Smith and Szathmary (1995); Sterelny (2001, 2004); Xu and Gordon (2003);
Paterson and Gray (1996); Sapp (1994); Umesaki et al. (1997).
sensitivity or an olfactory aversion to apples. This supposition is supported by
behavioral tests, in which the apple variant accepts both apples and haws as hosts,
whereas only a small percentage of the haws variant apples and most show a strong
preference for haws (Prokopy et al. 1998; Luna and Prokopy 1995). As indicated by
single-host acceptance tests, the apple reared flies show a greater percentage of egg
laying behavior on the apple host than do the hawthorn-reared flies. Thus, the
familiarity-inducing rearing experience (exposure learning) makes the apple-reared
flies more accepting of the apple host, although they still have a preference for the
hawthorn host. Given the ecological circumstances, the increased likelihood of
acceptance of the apple host, even in the face of a preference for hawthorn, would
perpetuate the transgenerational courting, mating, and laying of eggs in apple
orchards. Apple maggot flies hatch out at the base of the tree in which their mother
laid eggs the previous summer (Prokopy and Bush 1993, p. 6). As they mature
sexually, the flies may wander tens or hundreds of yards, but they remain in the
vicinity of the apple orchard, if not in the orchard itself. The scent of the apples
attracts them. Due to this early rearing experience rendering the apple scent
acceptable, the cycle renews itself because of the high probability that the early
maturing apple fly will encounter the odor of apples rather than hawthorns. In support
of incipient speciation, the two variants are not genetically somewhat distinct and do
not interbreed freely in nature, although they are morphologically the same and
remain interfertile. (Gottlieb 2003, pp. 17-19).
This case discussed by Gottlieb is interesting not only because it has been studied in detail but
also because it shows how inheritanceD can be the result not of a single mechanism but rather
of the interaction between different mechanisms. The apple variant and the hawthorn variant
of the maggot fly have many reliably reoccurring phenotypic differences: the apple variant
mates and breeds on apples while the hawthorn variant mates and breeds on hawthorns, the
apple variant hatches in the summer while the hawthorn variant hatches in the fall, etc. These
differences are kept in place by a complex interaction of genetic and non-genetic
mechanisms. First of all, there is the fact that the apple variant doesn’t have olfactory
aversion to apples, while the hawthorn variant does. Even though Gottlieb tells us nothing
about the developmental origins of this difference, we can suppose that genes may have
something to do with this difference. We can suppose that it is partly because of genetic
differences that some flies could shift to apples while others couldn’t. Such genetic
differences – if they exist – are kept in place by genetic transmission. Second, there is the fact
that exposure learning can affect the likelihood that a fly will accept a particular tree as a site
for mating, breeding, and ovipositioning. Because of this mechanism, similarly to what
happens in the case of the lucky butterfly, flies that hatch on apples are much more likely to
select apples as their oviposition site than flies that do not hatch on apples. Obviously, flies
with an aversion to apples are unlikely to undergo this kind of exposure learning. Third, there
is the fact that apples mature earlier than haws. Because of this, flies that hatch on apples are
unlikely to encounter and be influenced by the scent of haws, and vice versa. This increases
the likelihood that, when they have to choose an oviposition site, the flies will stick to the
kind of plant on which they hatched and that they experienced early in life. Given all this, the
reliably reoccurring phenotypic differences between the apple variant and the hawthorn
variant can be seen as the result of three interacting processes: (1) genetic transmission of
DNA sequences that affect olfactory preferences, (2) exposure learning that affects
preferences in the selection of a site for mating, breeding, and ovipositioning, and (3)
differences in maturation timing between apples and haws (an external ecological factor).
Because of the structure and complexity of the genome and because of the way it mutates,
genetic variation affects very many phenotypic traits, and it does so in all species, including
the human species. This suggests that most cases of reliably reoccurring phenotypic variation
involve reliably reoccurring genetic variation. But this is very different from saying that all
cases of reliably reoccurring phenotypic variation involve reliably reoccurring genetic
variation only. It may or may not be true that inheritanceD always involves genetic
transmission, but it is certainly not true that it always involves genetic transmission and
nothing else. The examples discussed above show that there exist many important nongenetic mechanisms capable of producing inheritanceD. There exist many mechanisms that
generate the reliable reoccurrence of differences in non-genetic developmental factors and
thereby the reliable reoccurrence of non-genetically-caused phenotypic differences.10
Another reason why the example discussed by Gottlieb is interesting is that it illustrates that
the reliable reoccurrence of phenotypic variation generated by mechanisms other than genetic
transmission can not only be the target of natural selection but also be the origin of speciation
events, including (importantly) events of sympatric speciation.
4. Conclusions
We can distinguish between genetic inheritanceD (genetic transmission) and non-genetic
inheritanceD (all the processes other than genetic transmission that cause the reliable
reoccurrence of variant developmental factors and thereby the reliable reoccurrence of
phenotypic variation). The received view in biology doesn’t recognize the existence of nongenetic inheritanceD (at least not in general, and with the exception of cultural inheritance).
This is either the result of believing in the DNA-centric theory of inheritanceF or the result of
Dawkins-style assumptions about non-genetic developmental factors and the way they affect
phenotypic variation. Either way, the received view is incorrect. The DNA-centric theory of
inheritanceF is wrong because the reliable reoccurrence of phenotypes requires the reliable
reoccurrence of both genetic and non-genetic factors. Dawkins-style assumptions are wrong
because it’s not true that non-genetic developmental factors are either invariant or such that
the distribution of the variants in one generation is uncorrelated with the distribution of the
variants in the next generation. Hence, the DNA-centric theory of inheritanceD must be
abandoned in favour of a more pluralistic theory that appeals both to genetic and non-genetic
mechanisms.
Obviously, there exist important differences between genetic and non-genetic inheritanceD.
Non-genetic inheritanceD is a very heterogeneous set of processes, each of which may occur
only in a very limited set of lineages, or may affect only some very specific cases of reliably
reoccurring phenotypic variation. In contrast, genetic inheritanceD is a single process (genetic
transmission) that plays a pervasive role in the reliable reoccurrence of phenotypic variation
in very many different cases and lineages.11 This fact may be in part explain why biologists
have concentrated on genetic inheritanceD and why (with few exceptions) they have ignored
non-genetic inheritanceD.12 But, in order to gain a proper understanding of evolutionary
phenomena, it’s important to study both kinds of processes, the ways they differ, and the way
their interactions affect the evolutionary process.13
10
One should always distinguish between the mechanisms that cause the reliable reoccurrence of variant
developmental factors (which can be genetic and non-genetic) and the developmental factors themselves (which
can also be genetic and non-genetic). Mechanism other than genetic transmission (such as assortative mating) can
for example be involved in the reliable reoccurrence of genetic differences (Mameli 2005).
11
Some of the differences between genetic and non-genetic inheritanceD that may have important consequences
for the evolutionary process are mentioned and briefly discussed in Mameli (2004); see also Avital and Jablonka
(2001); Jablonka (2001); Sterelny (2001, 2004); Odling-Smee et al. (2003).
12
Jablonka and Lamb (1999); Avital and Jablonka (2001); Jablonka (2001, 2004); Gray (1992, 2001); Griffiths
and Gray (1994, 1997, 2001); Gottlieb (2003); Sterelny (2001, 2004); Sterelny et al. (1996); Sapp (1987, 1994,
2003); Immelmann (1975); Odling Smee et al. (2003); Mousseau and Fox (1998).
13
Thinking about the genetic and non-genetic mechanisms responsible for the transgenerational stability of
phenotypic differences may be important not only in the context of understanding how selection can act at the
level of the individual, but also in the context of understanding how selection can act at the group level. The
concept of inheritanceD can be applied to the groups as well as to individuals. Boyd and Richerson (2005) argue
that genetic transmission is not capable of keeping variation between human groups into existence
transgenerationally and that, in contrast, conformity biases and altruistic punishment may be capable to do so when
Acknowledgements: Many thanks to Peter Carruthers, Stephen Laurence, and Stephen Stich
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Maynard Smith, Kim Sterelny, David Papineau, Paul Griffiths, Russell Gray, Peter
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P
G
P
G
P
G
Fig. 1 – The DNA-centric theory of inheritanceF. ‘G’ stands for ‘genes’; ‘P’ stands for
‘phenotypes’.
E
E
P
G
E
P
G
P
G
Fig. 2 – The pluralistic (non-DNA-centric) theory of inheritanceF. ‘E’ stands for some nongenetic developmental factors that – by reliably reoccurring or by persisting – contribute to
the reliable reoccurrence of some phenotypes. The parental phenotype can also be involved in
the reliable reoccurrence of phenotypic features; this is represented by the horizontal arrows
in the middle.