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Inheritance Systems
First published Wed Jan 4, 2012
Organisms inherit various kinds of developmental information and cues from their parents. The
study of inheritance systems is aimed at identifying and classifying the various mechanisms and
processes of heredity, the types of hereditary information that is passed on by each, the functional
interaction between the different systems, and the evolutionary consequences of these properties.
It is now common to identify heredity with the transmission of genes, or even more concretely with
the transmission of DNA sequence, from parents to offspring. It is, however, clear on reflection that
there are other ways in which offspring may receive from parents resources or cues that affect their
development. This is particularly apparent in humans, and the suggestion that social and cultural
cues may serve as an additional “inheritance system” has been made many times. These
observations, and the models of dual inheritance of genes and culture (e.g., Boyd & Richerson
1985; Cavalli-Sforza & Feldman 1981; Durham 1991), are a useful starting point from which to
approach the more general project of elucidating the notion of inheritance system. Cultural
inheritance, however, is a broad category, whereas the analysis of inheritance systems discussed
below tends to be more fine-grained (see Sterelny 2001, p. 337). The term “inheritance systems” is
used to describe different mechanisms, processes, and factors, by which different kinds of
hereditary information are stored and transmitted between generations.
We present the discussion of inheritance systems in the context of several debates. First, between
proponents of monism about heredity (gene-centric views), holism about heredity (Developmental
Systems Theory), and those stressing the role of multiple systems of inheritance. Second, between
those analyzing inheritance solely in terms of replication and transmission, and views that stress the
multi-generation reproduction of phenotypic traits. A third debate is concerned with different
criteria that have been proposed for identifying and delimiting inheritance systems. A fourth
controversy revolves around the significance of the “Lamarckian” aspects of some of the
inheritance systems that have been identified, such as epigenetic inheritance and behavioral
inheritance, that allow the transmission of environmentally induced characters (i.e., “soft
inheritance”).
This entry is organized as follows: Sections 1 and 2 provide common ground and historical context
for the discussion. Section 3 discusses specific accounts of inheritance systems. General
evolutionary implications are presented in section 4. Finally, section 5 summarizes some of the
open questions in the field.
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1. Introduction
o 1.1 Early Work On Non-Genetic Inheritance
o 1.2 Monism, Holism, and Multiple Systems views
o 1.3 Heredity and Inheritance
o 1.4 Variation, Hereditary Variation, and Inheritance Systems
2. Reproduction and Replication
o 2.1 Multi-generation reproduction of phenotypes
o 2.2 Inheritance and replication
o 2.3 The reproducer concept
o 2.4 Inheritance systems and notions of information
3. Classification of Inheritance Systems
o 3.1 Inheritance Channels
o 3.2 Identifying and delimiting inheritance systems
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3.3 Jablonka's and Lamb's Classification of Inheritance Systems
3.4 Niche Construction Theory and Ecological Inheritance
4. Developmental and Evolutionary Implications
o 4.1 Units of Selection
o 4.2 Scaffolding
o 4.3 The ontogeny of inheritance systems
o 4.4 Assimilation
o 4.5 Regulation and control
o 4.6 Evolution of Inheritance Systems
5. Conclusions
Bibliography
Academic Tools
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Related Entries
1. Introduction
1.1 Early Work On Non-Genetic Inheritance
Biologists have long known of patterns of inheritance, and eventually of inheritance mechanisms,
that go beyond genetic inheritance (Jablonka & Lamb 2005; Sapp 1987). Two fundamental types of
arguments led to this conclusion: arguments based on observations regarding patterns of
inheritance, and arguments concerned with the localization of hereditary factors inside cells.
Arguments of the first kind were based on hereditary relations and inheritance patterns that fail to
conform to the rules of Mendelian inheritance (e.g., maternal inheritance). If Mendelian inheritance
patterns are the result of the way the chromosomes in the eukaryotic cell nucleus behave, nonMendelian heredity must depend on separate inheritance processes, mechanisms, or systems (Beale
1966; Sager 1966). Second, there were observations of hereditary phenomena that seemed to
depend on factors residing in the cytoplasm of cells, rather than their nucleus, where the genetic
material is localized. The interpretation of these observations was highly contested (Darlington
1944; Sapp 1987).
Today, we know that some of these observations are related to the (maternal) inheritance of
organelles residing in the cytoplasm, such as the mitochondria and chloroplasts, organelles which
carry their own DNA. This however does not encompass all the mechanisms which underlie
cytoplasmatic inheritance. Paradigmatic work on cytoplasmatic inheritance done by Sonneborn,
Beale, Nanney, and their colleagues in the 1950s and 1960s, was concerned with patterns of
inheritance in unicellular organisms, and in particular the protist genus Paramecium. It was
suggested that the self-sustaining regulatory loops that maintain gene activity or inactivity in a cell
would persist through cell division, provided the non-DNA components of the system (many of
which reside in the cytoplasm in eukaryotic microogranisms) were shared among daughter cells. In
this way, alternative regulatory phenotypic states would be inherited. Among the properties whose
inheritance was studied were mating-type variations, serotype variations, and the structural or
“surface inheritance” of ciliary structures. Remarkably, microsurgical changes to the ciliary
structures on the surface of Paramecium cells are inherited by offspring. The stability of induced
characters once the stimulus was removed (called “cellular memory”) and the number of
generations characters were maintained varied widely. However, the results indicated that long-term
stability and heritability need not be the result of changes to the DNA sequence (Nanney 1958).
During the 1950s to 1970s a growing set of observations indicated that determined and
differentiated states of cells are transmitted in cell lineages. These observations concerned studies of
Drosophila imaginal discs by Ernst Hadorn; Briggs and King's cloning experiments with
amphibians; Mary Lyon's work on X-chromosome inactivation; and work establishing the in vitro
clonal stability of cultured cell lines. Eventually, the term epigenetic inheritance came to refer to
hereditary variation that does not involve changes to the DNA sequence.
The brief account of some of the early work on unicellular organisms given above illustrates some
of the distinctions that are elaborated in the rest of this entry. One group of questions is concerned
with the properties of hereditary relations, the sources of variations (in particular, whether they can
be environmentally induced), the stability of variations and their regulation, and so on. A second
class of questions is concerned with the way hereditary information is stored and transmitted. It is
here that we can locate the debates about nuclear versus cytoplasmatic inheritance and about the
primacy of DNA as the information store of the cell.
1.2 Monism, Holism, and Multiple Systems views
The increasing focus by biologists on DNA as a “master molecule” containing coded genetic
information, after the discovery of the double helix structure in 1953, on the one hand, and the
gene-selectionist view articulated in 1966 by George Williams in his book Adaptation and Natural
Selection, which culminated in the “replicator” concept in philosophy of biology (Dawkins 1976;
Hull 1980, see entry: Replication), on the other, led to a tendency to view biological inheritance as
consisting of a single channel of transmission. This channel is understood to involve the inheritance
of genetic information encoded in DNA (or, in some viruses in RNA), a view often referred to as
“geno-centrism”. It should be noted that the replicator concept itself does not rule out non-genetic
replicators (Dawkins 1976, see also the discussion by Sterelny, Smith, & Dickison 1996). The dualinheritance model of biological and cultural evolution which is based on two types of replicators,
genes and memes, is a paradigmatic example that is based on the replicator framework, and that
involves both more than one channel of inheritance and non-genetic inheritance (e.g., Blackmore
1999). Accounts of heredity that are based on the notion of replicators may approach non-genetic
inheritance by characterizing multiple kinds of replicators (e.g., memes), each of which is supposed
to underlie a different channel of non-genetic inheritance. John Maynard Smith and Eörs Szathmáry
account of Major Transitions in Evolution is organized around transitions to new kinds of ways in
which information is stored and transmitted, understood as transitions to new kinds of replicating
entities (Maynard-Smith & Szathmáry 1995), and multiple types of replicators are embraced by the
notion of the extended replicator (Sterelny 2001; Sterelny et al. 1996) discussed below. More
typically, however, non-genetic forms of inheritance, with the exception of cultural inheritance in a
few groups of higher animals, are often ruled out as not fulfilling the requirements imposed by the
definition of a replicator. It should be emphasized that the replicator view posited replicators,
typically genes, as the unit of selection; the work discussed in this entry is concerned with the
biological processes and mechanisms involved in inheritance, and is not concerned directly with the
debate about the unit of selection. Implications regarding selection are elaborated in section 4.1.
Approaches that rule out or ignore non-genetic inheritance might be characterized as “monist” in
their treatment of the question of the existence and significance of multiple inheritance systems.
Monist tendencies may be traced back already to Wilhelm Johannsen's work at the beginning of the
20th century. While Johannsen invented the term “gene” in order to remain uncommitted to a
specific view about the material constitution of hereditary factors, both this term and the notion of
“genotype” that he developed suggest a monist view of inheritance. This tendency was reinforced
by molecular genetics and the replicator framework.
How do monist views handle the other forms of inheritance that are known to exist? Consider the
mitochondria. Monist accounts regard the maternal inheritance of organelles such as the
mitochondria, which might conceivably be thought to constitute a separate inheritance channel, if
not system, to be of marginal conceptual importance. First, it can be argued that being based on
genetically coded information (DNA sequence), the similarities with nuclear inheritance allows it to
be seen as not involving a distinct inheritance system, if this notion is understood to refer to the way
hereditary information is stored and transmitted. Indeed, views that focus on multiple inheritance
systems, may for the same reason not consider the inheritance of plastids as based on a distinct
inheritance system. Second, it is assumed that the evolution of complex organismal traits is to be
explained by natural selection affecting the genetic information in the nucleus. Thus, mitchondrial
inheritance, and plastid inheritance more generally, are considered to be of limited explanatory
value when trying to give a general account of the evolution of the organism (beyond the early
stages of endosymbiogenesis), and is of interest mainly when considering the evolution of the
mitochonrdia themselves, in which case there is yet again a single inheritance system that is
relevant, that of the mitochondrial genome. Similar reasoning is applied more generally to reject
forms of supposedly extra-genetic inheritance that are not based on the transmission of DNA, by
claiming either that the inheritance fails to be the transmission of information or that the
information that can be transmitted is limited and thus not evolutionarily significant, and is merely
the transmission of material resources or infrastructure. Cashed out in the terms of the replicator
framework, arguments against supposed cases of extra-genetic inheritance are that they do not lead
to the establishment of replicators, which are entities that are faithfully copied and passed down
multiple generations, yet replicators are necessary for evolution by natural selection, or that extragenetic inheritance leads to replicators that are limited in the repertoire of variants they support (see
Godfrey-Smith 2000). Proponents of the multiple inheritance systems view and of holistic views
about inheritance argue that these requirements are either unnecessary or too strong, and lead to a
distorted understanding of evolution (see Griffiths & Gray 2001; Jablonka 2001).
In contrast to monist views, proponents of “Developmental Systems Theory” (DST) (Griffiths &
Gray 1994, 2001) offer a radical reformulation of evolutionary theory, including the notion of
inheritance and the treatment of extra-genetic inheritance. DST applies the notion of inheritance to
any developmental resource that is reliably present in successive generations, and which is part of
the explanation of the similarity between generations (Griffiths & Gray 2001). While embracing the
existence of non-genetic inheritance, and its significance for evolutionary accounts, these
researchers argue against separating these phenomena into multiple channels or systems of
inheritance (Griffiths & Gray 2001): Inheritance phenomena are so intertwined in their effects on
development, and each relies on others to have its developmental effect, that it is both more realistic
and scientifically more productive not to separate them into distinct channels, systems, or replicator
types. The DST approach might be characterized as “holistic” in its treatment of inheritance.
In contrast to monism and holism, the views discussed in this entry identify and classify various
mechanisms and processes of inheritance, the types of hereditary information that are passed on by
each, the function and interaction of the different systems, and the evolutionary consequences of
these properties. Contemporary views on evolution that stress the role of multiple systems of
inheritance have been greatly influenced by the work Eva Jablonka and Marion Lamb, in particular
their arguments about the evolutionary role of epigenetic inheritance (Jablonka 2001, 2002;
Jablonka & Lamb 1995, 2005, 2006) . In addition to the line of work influenced by Jablonka and
Lamb, extra-genetic inheritance is stressed by DST, albeit in the form of holism about inheritance,
and in the “extended replicator” framework elaborated by Kim Sterelny et al. (Sterelny 2001;
Sterelny et al. 1996).
Responding to pressure from DST, the extended replicator approach elaborates the account of nongenetic replicators provided by the replicator framework (Dawkins 1976; Hull 1980) to include
non-genetic replicators, while retaining the replicator/interactor distinction which both the holism of
DST and the multiple systems view of Jablonka and Lamb reject: Replicators form lineages, while
interactors, through which replicators interact with the environment, are ephemeral (see section 2.2
for discussion). Sterelny et al. (1996) emphasize the distinction between genes as factors having “a
distinctive informational role in inheritance” and other reliably present developmental resources.
According to them, this distinctive informational role explains why genes, and not just any
resource, represent the phenotype and have a special developmental role. They embrace other cases
of biological replication if they can be informational in the strong sense their account demands. In a
nutshell, the main requirements are that the replicator have the biofunction (i.e., proper function or
evolutionarily selected function) of representing the phenotype (or aspects of it) and that it play a
causal role in the production of the phenotype. Genes according to this view do not have a unique or
privileged role in determining the phenotype; however, they do have a distinctive informational role
(see section 2.4). Whether other types of replicators exist is an empirical matter, and viewing
various biological processes as replication may be scientifically productive according to Sterelny et
al. (1996).
1.3 Heredity and Inheritance
It is useful to distinguish between the following terms. The terms heredity and hereditary will be
used henceforth to refer to reliable resemblance relations between parents and offspring. Particular
traits (phenotypic or genotypic), may be hereditary in this sense.[1] The term inheritance will be
used to refer to causal processes of transmission between parents and offspring that account for
heredity, and the mechanisms responsible for them. We might, for example, say that eye color is
hereditary, and that genetic inheritance accounts for the heredity of eye color (or, more formally, for
the heredity of variations in eye color). Multiple inheritance processes may be implicated in the
heredity of a particular phenotypic trait. Inheritance is often construed as transmission of
information, though this notion raises difficulties; this issue is discussed in section 2.4.
The terms parent and offspring are used in a general sense, since transmission may be from
individuals other than the genetic parents of the organism (i.e., non-vertical). Multiple inheritance
systems may lead to multiple “parent-offspring” relations.
1.4 Variation, Hereditary Variation, and Inheritance Systems
A fundamental requirement for evolutionary change via natural selection is the existence of
variation in the population. However, for variations to have evolutionary effect they need to be (at
least partly) hereditary or heritable (see entry on heritability; I will here focus on hereditary
variations and hereditary transmissibility as defined above, and will not discuss the notion of
heritability which is a population term). It is hereditary variations that fuel evolution through
natural selection (Lewontin 1970, 1985). Thus, if we aim to give a general account of possible
evolutionary change we may start by examining and classifying hereditary variations (Jablonka &
Lamb 2005). Hereditary variation, in turn, may be accounted for in terms of inheritance
mechanisms, hence by accounts of inheritance systems. As a starting point we can understand the
notion of inheritance system as referring to mechanisms, processes, and participating factors, that
are involved in transmission between parents and offspring leading to hereditary relations. Several
influential accounts of inheritance systems that are of philosophical interest are discussed in section
3.
2. Reproduction and Replication
Work on inheritance systems is often situated in the context of developmental evolutionary biology,
and attaches great significance to the ways in which inheritance interacts with the development of
phenotypes. This section contrasts this perspective on inheritance with views that focus on
replication. James Griesemer's reproducer notion which combines inheritance and development is
presented. Finally, the relationship between inheritance systems and notions of biological
information is discussed.
2.1 Multi-generation reproduction of phenotypes
In contrast to the replicator view that looks for reliably replicating entities that either produce copies
of themselves, induce the production of such copies, or pass on their structure through replication
processes (Dawkins 1976; Hull 1980), the views discussed in what follows see natural selection as
depending on the reliable multi-generation reproduction or reconstruction of phenotypes, and
conceptualize inheritance accordingly (for related discussion of the topics in this section and
historical details see the entry on replication). This perspective opens up many questions that the
discussion of inheritance systems attempts to address. First among these is how hereditary resources
or inheritance processes affect the development of offspring so as to reliably reconstruct parental
phenotypic characters; this question is shared more generally by developmental evolutionary
biology (Evo-Devo) and Developmental Systems Theory. Reconstruction typically occurs during
the development of the offspring, which is more or less independent from the parent, and may be a
complex, multi-stage, and temporally drawn out process. It may involve more than one inheritance
system and depend on interactions between inheritance systems, depend on persistent
environmental resources such as sunlight and gravity as well as environmental conditions produced
by organisms and interactions with them (niche construction), and depend on processes such as
pattern formation that give rise to what might be characterized as emergent properties. We now turn
to a discussion of inheritance thus construed vis-a-vis the notion of replication.
2.2 Inheritance and replication
As mentioned earlier, two major influences led to the emphasis on replication as a necessary
condition for evolution via natural selection: the influence of the replicator framework and the
discovery of the molecular basis of genetic inheritance, in particular DNA replication. In their 1953
paper on the structure of DNA, James Watson and Francis Crick famously noted that the properties
of the double helix structure suggest a straightforward method for replicating the DNA sequence. It
is now known that DNA replication is semiconservative: each of the strands of the double stranded
DNA molecule is used as a template for constructing a complementary strand, and the replication
process results in two DNA molecules, each containing one of the original strands and one newly
constructed strand. In the absence of mutations, each of the new double stranded DNA molecules
has the same sequence of base pairs (nucleotides) the original DNA molecule had. DNA replication
explains how the information in the DNA sequence is copied, so that when the cell divides each
daughter cell ends up with a complete copy of the original cell's DNA. This is a critical element of
genetic inheritance, though the genetic inheritance processes of mitosis and meiosis are far more
involved than DNA replication, which is only one component of them.
When considered from the perspective of accounting for the reliable reconstruction of parental
phenotypes, replication of the kind found in genetic inheritance is seen to be neither sufficient nor
necessary for heredity (Jablonka 2004, has a particularly clear discussion of these issues). The
inheritance of cellular properties as a consequence of self-sustaining metabolic loops, one kind of
cellular epigenetic inheritance, is an example of inheritance not involving replicators. Partly on the
basis of cellular epigenetic inheritance and similar observations about other forms of extra-genetic
inheritance, such as behavioral and linguistic transmission, that do not conform with the replicator
framework, Jablonka has argued that the replicator/interactor distinction should be rejected
(Jablonka 2001, 2004). More generally, she argued that “the replicator/vehicle dichotomy… is
meaningless in all cases in which the transmission of information or the generation of new heritable
information depends on development” (Jablonka 2001, p. 114). Godfrey-Smith (2009, sec. 2.4)
discusses formal arguments showing that replicators are not a necessary condition for evolution by
natural selection.
DNA replication is also not sufficient for explaining cellular heredity, since cellular heredity
depends on support from epigenetic nuclear and cytoplasmatic inheritance mechanisms that
maintain proper gene regulation. This point has been made during the historical debates about
cytoplasmatic inheritance (Nanney 1958; Sapp 1987). Moreover, cellular epigenetic inheritance is
essential for cell differentiation in multi-cellular organisms, which involves the establishment of
lineages of cells that produce tissue specific phenotypes that are not due to differences in DNA
sequence. Differentiated cells inherit their tissue-specificity, which they usually do not alter
throughout their life-cycle. This means that in addition to its role in cellular heredity, cellular
epigenetic inheritance is essential for the multi-generation reconstruction of phenotypes of multicellular organisms, regardless of any direct role transgenerational epigenetic inheritance plays in the
transmission of characters from parent to offspring above the cellular level, though such effects are
also well known (Jablonka & Raz 2009).
2.3 The reproducer concept
James Griesemer has proposed the reproducer as a fundamental notion for thinking about
reproduction in evolution. A reproducer is an entity that multiplies with material overlap between
parent and offspring, transferring mechanisms conferring the capacity to develop the capacity to
reproduce (Griesemer 2000a, p. S361, 2000b, 2000c, see also the entry on replication Section 7). By
definition, being a reproducer is a property applicable to systems that have developmental
capacities. In contrast with traditional accounts of natural selection that focus on heredity,
Griesemer's analysis of reproduction processes attempts to integrate heredity and development in a
single conceptual scheme. Godfrey-Smith has argued that both requirements emphasized by
Griesemer — material overlap between generations, and the capacity to develop — are too strong,
and are not required for a formal account of evolution via natural selection per se (Godfrey-Smith
2009, pp. 83-84).
Based on the reproducer concept, Griesemer has proposed an analysis of modes of multiplication in
which reproduction, inheritance, and replication are special cases of multiplication processes
(Griesemer 2000a, p. S360, 2000c). According to this classification, inheritance processes are
reproduction processes in which there are evolved mechanisms for producing hereditary relations in
development. Replication processes in turn are inheritance processes with evolved coding
mechanisms. Thus, replication (which is contrasted by Griesemer with mere copying) is a special
case of inheritance, itself a special cases of biological reproduction. Genetic inheritance is a
replication process and as such it involves coding mechanisms. Since genes do not constitute
mechanisms of development in their own right, but are pieces of mechanisms, Griesemer argues
that they cannot have the privileged explanatory role often accorded to them (Griesemer 2000a, p.
364). According to Griesemer's classification, epigenetic inheritance processes can be classified as
inheritance processes which are not replication processes (Griesemer 2000c, p. 250).
Griesemer's classification of reproducers is an abstraction hierarchy. It provides a formal taxonomy
of reproducers, arranging them in a series of nested classes. The classification of inheritance
systems suggested by Jablonka and Lamb (Jablonka 2001; Jablonka & Lamb 2005) discussed in the
next section, in contrast, enumerates types of concrete inheritance systems found in the living
world.
2.4 Inheritance systems and notions of information
It is tempting to try and apply the notion of information to the study of inheritance systems in
general, and extra-genetic inheritance in particular, since on an abstract level inheritance may be
thought of as transmission of information or informational resources from parent to offspring (as
opposed to the transmission of material resources). However, it is notoriously difficult to come up
with notions of information that are suitable for studying the various aspects of biological
phenomena (see the entry on biological information for a survey) and a fair amount of skepticism
may be in order.
A common argument in favor of treating genetic inheritance as having a unique developmental role
is the claim that genes play an informational role, not shared by other hereditary developmental
resources. The holistic view of inheritance articulated by Developmental Systems Theory
downplays the significance of the idea that inheritance should be conceived as the transmission of
information between generations (Griffiths & Gray 2001; Sterelny 2001, p. 334, see also the
discussion in Sterelny et al. 1996, p. 379). In particular, DST uses the so-called parity argument to
reject the view that DNA is uniquely informational while other inherited resources merely provide
material support for reading or interpreting DNA (Griffiths & Knight 1998).
Jablonka (Jablonka 2001, 2002) introduced her discussion of inheritance systems by characterizing
them as systems that carry hereditary information, which in turn she defined as “the transmissible
organization of an actual or potential state of a system” (cf. the different notion of information and
representation favored by Sterleny et. al. 1996). A common framework for discussing hereditary
information can then be used to compare and analyze various inheritance systems and expose their
differences as well similarities (see section 3.3).
3. Classification of Inheritance Systems
It is now fairly common in biological discourse to talk about various forms of inheritance in
addition to genetic inheritance. The two type of inheritance most often referred to are probably
cellular epigenetic inheritance and cultural and behavioral inheritance in humans and various
animals. There is however no standardized or de facto system or nomenclature used to classify
inheritance systems and their properties. This is partly due to the wide range of hereditary
phenomena and the debates described earlier. A principled taxonomy would provide a guide for
identifying inheritance systems, delimiting them from one another, comparing their properties and
possible functions, and so on.
This section begins by making clear the distinction between inheritance systems and channels of
inheritance. Various criteria that have been proposed for identifying inheritance systems are then
presented. The section concludes with a detailed discussion of the influential account of inheritance
systems presented by Jablonka and Lamb and a discussion of ecological inheritance and niche
construction.
3.1 Inheritance Channels
A fundamental distinction between inheritance channels and inheritance systems should be made
before classifying inheritance systems. Simply put, inheritance channels refer to “routes across
generations” (in the words of Sterelny et al. (Sterelny et al. 1996, p. 390)) through which hereditary
resources or information pass from parent to offspring. The notion of inheritance system, in
contrast, as used by Jablonka and Lamb in particular, is meant to classify inheritance factors,
mechanisms, and processes, and the ways in which they store and carry hereditary information
(Jablonka 2001; Jablonka & Lamb 2005).
Multiple inheritance channels may be involved in the reconstruction of the phenotype. For example,
as noted in the discussion of cellular heredity, inheritance of organelles during cell division is
required for the survival of daughter cells in addition to the inheritance of the nuclear genome. The
role of multiple channels is particularly apparent in cases where phenotypes depend on symbiotic
associations and thus on the transmission of symbionts. Examples of transmission of symbionts
include: (1) The transmission of gut bacteria, which are required for digestion and for normal
intestinal development, from mother to offspring. (2) Fungus-growing ants depend on the
cultivation of fungus for food in underground gardens. When new queens leave their parent
colonies, they carry a fragment of the fungus with them to the site of the new colony. (3) Various
species of aphids, clams, and sponges allow some bacteria to pass through the oocytes from parent
to offspring, leading to vertical transmission parallel to genetic transmission. As a final example of
multiple channels of inheritance note that cultural transmission in humans and animals, which is
required for the reconstruction of behavioral phenotypes such as bird songs, food preferences, and
other cultural traditions (Avital & Jablonka 2000), may also be considered to constitute
supplementary inheritance channels.
The same inheritance system may be involved in more than one inheritance channel. For example,
the genetic inheritance system as defined by Jablonka and Lamb is responsible for the inheritance of
the information in the DNA in the eukaryotic nucleus and in the DNA of mitochondria. Horizontal
gene transfer more generally is considered by Jablonka and Lamb to belong to the genetic system
(Jablonka & Lamb 2005, p. 233), though it typically involves additional vectors or transmission
channels. Conversely, a single inheritance channel may involve multiple inheritance systems, in the
sense used by Jablonka and Lamb. While many interesting cases involve identifying new
inheritance channels which are based on new inheritance systems, and discussions are often
ambiguous as to which of the two notions they refer to, the study of inheritance systems is a
separate endeavor from the analysis of the inheritance channels affecting individual organisms or
traits. The holistic view about inheritance, found in Developmental Systems Theory, rejects both the
analysis of inheritance in terms of multiple systems and in terms of multiple channels, arguing that
both distinctions are at most convenient idealizations (Griffiths & Gray 2001), and it is not unusual
for debates about holism to conflate the discussion of the two issues.[2]
In response to the DST rejection of multiple channel accounts of inheritance, Griesemer et al.
(2005) note the multiple ways in which channels can be independent from one another. Channels
may be individuated as separate channels physically, chemically, or biologically, regardless of
whether they are statistically independent information channels. Additionally, causal independence
should not be required for individuating inheritance channels. While Jablonka and Lamb use a
notion of biological information to characterize inheritance systems, they are not individuated based
on statistical independence, but rather mechanistically (or, more more accurately, mechanismically,
that is by identifying classes of inheritance mechanisms) and by biological function.
3.2 Identifying and delimiting inheritance systems
As it is hereditary variations that are needed for evolution via natural selection, Jablonka and Lamb
set out to study different inheritance systems (where system is understood roughly to mean a set of
interacting factors and mechanisms) by identifying different kinds of hereditary variation (Jablonka
2001; Jablonka & Lamb 1995, 2005). Their approach can be described as focused on the
mechanismic basis for different types of hereditary phenotypic variation. They have identified
multiple inheritance systems, each with several modes of transmission, that have different
properties, and that interact and coevolve (Jablonka 2001, p. 100; Jablonka & Lamb 2005). The
systems are said to carry information, defined as the transmissible organization of an actual or
potential state of a system. A detailed account of their influential classification is presented in
section 3.3.
A different approach to characterizing and possibly for identifying and delimiting inheritance
systems posits that to count as an inheritance system a system has to have evolved for the purpose
of transmitting hereditary information, i.e., to have the “meta-function” of producing heritable
phenotypes (Shea 2007). In this respect this approach is reminiscent of the extended replicator
approach of Sterelny et al. (1996). Other requirements that have been proposed in the literature are
the demand for “unlimited” heredity, i.e., unlimited repertoire of variants the system can store and
transmit, needed for sustained or cumulative evolution (see discussion in Godfrey-Smith 2000;
Maynard-Smith & Szathmáry 1995, p. 43), and the ability to generate fine-grained response to
selection (see Griffiths 2001, p. 460). Both these requirements regard genetic inheritance as having
a privileged role in development and evolution in comparison with epigenetic inheritance processes.
Jablonka and Lamb address these concerns with evolvability by noting that multiple instances of
limited systems of inheritance may exist within one cell (e.g., multiple self-sustaining metabolic
cycles), thus extending the repertoire of hereditary variations, and by emphasizing the effects
limited hereditary systems can have on the evolution of genetic variations (see the discussion of
genetic assimilation below). Jablonka also argues that the requirement for high fidelity of
replication (e.g., Sterelny 2001) is not as necessary for inheritance systems that employ filtering
mechanisms that ensure that transmitted variations are typically adaptive (Jablonka 2002). For
further discussion of the requirement for evolvability see the discussion of Sterelny's Hoyle
conditions in section 4.6.
It should be noted that all the properties discussed above are properties of systems, not properties of
particular hereditary relations, of particular transmission events, or of replicator tokens.
3.3 Jablonka's and Lamb's Classification of Inheritance Systems
Jablonka and Lamb characterize four broadly defined inheritance systems: two fairly specific
inheritance systems — the genetic inheritance system and the symbolic inheritance system found in
human languages — and two classes of inheritance systems — cellular and organismal epigenetic
inheritance systems and behavioral inheritance systems. The systems are classified and grouped
according to the way they store and transmit variations and by the properties of the hereditary
relations they give rise to.
Recently, Helanterä & Uller (2010) analyzed the inheritance systems Jablonka and Lamb identified
based on their evolutionary consequences. They claim that Jablonka's and Lamb's mechanismic
classification does not match a classification of means of inheritance according to their evolutionary
properties, and suggested classifying them into three categories: vertical transmission which covers
cases in which traits are transmitted from parent to offspring such as genetic inheritance and some
epigenetic phenomena; induction which covers cases in which the environment determines change
between parent and offspring such as induced genetic mutations and maternal effects; and
acquisition which covers cases in which traits originate from non-parental individuals or other
sources, for example horizontal gene transfer and various forms of learning.
The properties of the inheritance systems that Jablonka and Lamb chose to study are those they
deemed to be most pertinent for understanding inheritance, and its evolutionary consequences
(Jablonka 2001, p. 100). In more recent work Jablonka and Lamb (2005) distinguish between
properties of the way information is reproduced, and properties related to whether variation is
targeted, responsive to the environment, or otherwise biased (the so-called “Lamarckian
dimension”). Among the properties of reproduction of information that they identify are whether
reproduction results from ordinary cellular activity and relies on general purpose cellular
mechanisms or whether a dedicated copying system (i.e., cellular machinery) exists; whether the
inheritance system can transmit latent (unexpressed) information or is information necessarily
expressed phenotypically; and whether information is transmitted solely to offspring (referred to as
vertical transmission) or to neighbors as well (horizontal transmission).
The properties related to targeting, constructing, and planning of transmitted variation that Jablonka
and Lamb identify are:
1. Is variation targeted, in the sense that the production of variants is biased towards producing
some possible variants (i.e., “non-random”)?
2. Is variation subject to developmental filtering and modification before transmission, as
found for example in behavioral inheritance?
3. Is variation constructed through direct planning by the organisms?
4. Can variations change the selective environment, for example by changing the
environmental niche the organism occupies?
We now describe in more detail each of inheritance systems Jablonka and Lamb identified.
Jablonka's and Lamb's analysis of inheritance systems is summarized in tables 1 and 2.
Table 1: The reproduction of information
Inheritance
system
Genetic
Organizations
of information
Modular
Dedicated
copying
system?
Yes
Transmits latent
Directions of
(nonexpressed)
transmission
information?
Range of
variation
Yes
Mostly vertical Unlimited
No
Limited at the
loop level,
Mostly vertical
unlimited at
the cell level
No
Limited at the
structure
Mostly vertical level,
unlimited at
the cell level
Epigenetic
Self-sustaining
Holistic
loops
Structural
templating
Holistic
RNA silencing Holistic
Chromatin
marks
Modular and
holistic
Organism-level
developmental Holistic
legacies
No
No
Vertical and
sometimes
horizontal
Limited at the
single
transcript
level,
unlimited at
the cell level
Yes (for
Sometimes
methylation)
Vertical
Unlimited
No
Mostly vertical Limited
Yes
Sometimes
No
Table 1: The reproduction of information
Inheritance
system
Organizations
of information
Dedicated
copying
system?
Transmits latent
Directions of
(nonexpressed)
transmission
information?
Range of
variation
Behavioral
Behavioraffecting
substances
Holistic
Nonimitative
Holistic
social learning
No
Limited at the
single
Both vertical behavior
and horizontal level,
unlimited for
lifestyles
No
No
Limited at the
single
Both vertical behavior
and horizontal level,
unlimited for
lifestyles
No
Imitation
Modular
Probably
No
Both vertical
Unlimited
and horizontal
Symbolic
Modular and
holistic
Yes, several
Yes
Both vertical
Unlimited
and horizontal
Table 2: Targeting, constructing, and planning transmitted variation
Variation
Variation subject to
constructed
Inheritance
developmental filtering
through
system
and modification?
direct
planning?
Generally not,
Usually not, although
except for the
expressed genetic
directed changes that changes may have to
survive selection
No
Genetic are part of
development and the between cells prior to
various types of
sexual or asexual
interpretive mutation reproduction
Variation is
targeted (biased
generation)?
Yes, a lot of
epigenetic variations
Epigenetic are produced as
specific responses to
inducing signals
Yes, selection can occur
between cells prior to
reproduction; epigenetic
No
states can be modified or
reversed during meiosis
and early embryogenesis
Yes, because of
Yes, behavior is selected
emotional, cognitive,
and modified during the No
Behavioral
and perceptual
animal's lifetime
biases
Variation can change
the selective
environment?
Only insofar as genes
can affect all aspects
of epigenetics,
behavior, and culture
Yes, because the
products of cellular
activities can affect the
environment in which
a cell, its neighbors,
and its descendants
live
Yes, new social
behavior and traditions
alter the social and
sometimes also the
Table 2: Targeting, constructing, and planning transmitted variation
Variation
Variation subject to
constructed Variation can change
Inheritance
developmental filtering
through
the selective
system
and modification?
direct
environment?
planning?
physical conditions in
which an animal lives
Yes, very extensively,
Yes, because
Yes, at many by affecting many
emotional, cognitive, Yes, at many levels, in
levels, in many aspects of the social
Symbolic
and perceptual
many ways
ways
and physical
biases
conditions of life
Variation is
targeted (biased
generation)?
(The tables above are reproduced with permission from Eva Jablonka and Marion J.Lamb,
Evolution In Four Dimensions: Genetic, Epigenetic, Behavioral, And Symbolic Variation In The
History Of Life, published by The MIT Press. 2005)
3.3.1 The Genetic Inheritance System (GIS)
The genetic inheritance system (GIS) uses the nucleotide sequence in nucleic acids, typically DNA,
to store and transmit information (i.e., hereditary variation), and includes the machinery responsible
for DNA replication, error correction etc. The GIS uses encoded information, as nucleotide
sequences code for amino acids that form proteins using the genetic code which specifies which
amino acid corresponds to each triplet of nucleotides (called a codon). The DNA sequence also
specifies functional RNA molecules. DNA nucleotides can be modified independently of each
other, a property referred to as modular organization; it has been argued that coded information
requires modular replication (Szathmáry 2000). Generally speaking, the genetic system provides
unlimited heredity, since the nucleotide sequence is not limited in size, and each position in it can
contain any nucleotide. These, particularly the claim that the sequence length is unconstrained, are
of course idealized assumptions. Unlimited heredity and modularity are most often attributed to the
genetic system as a whole, not only to protein coding regions, and it is often argued that they are
unique to it. Like the GIS, the symbolic inheritance system (discussed below), which is restricted to
human beings, exhibits unlimited and modular heredity.
Various kinds of regulatory regions in DNA are spread throughout most genomes. They comprise
“non-coding” sequences, in the sense that they do not code for proteins and do not depend on the
genetic code. Regulatory regions affect gene expression and chromatin dynamics. It is still debated
in the scientific community whether there are general properties of sequence organization that
determine these functions, which would suggest a high-order code. It should be noted that various
non-coding sequences interact in specific ways with epigenetic mechanisms (such as DNA
methylation and histone modifications) in order to produce their regulatory effects. The genome
which is the seat of genetic information is also a focal point for the operation of critical epigenetic
mechanisms, and it may turn out not to be possible to fully understand the properties of the genetic
inheritance system and its evolution in isolation from epigenetic inheritance (Jablonka & Lamb
2008; Lamm 2011).
Some mechanisms that generate variation in DNA are invoked in particular conditions (e.g., stress
conditions), and produce variation that is non-random in location and/or pattern (e.g., Levy &
Feldman 2004; reviewed in Jablonka & Lamb 2005, chap. 3). However, it is widely perceived that
most genetic variations are the result of non-directed processes that are not responsive to specific
inducing conditions.
3.3.2 Epigenetic Inheritance Systems (EISs)
Epigenetic inheritance occurs when environmentally-induced and developmentally-regulated
variations, or variations that are the result of developmental noise, are transmitted to subsequent
generations of cells or organisms (Jablonka & Lamb 2005). The term epigenetic inheritance is used
in a broad sense and in a narrow sense. The narrow sense refers to the systems that underlie cellular
heredity. Four EISs in the narrow sense are discussed by Jablonka and Lamb (2005): (1) Selfsustaining steady-states of metabolic cycles. Transmission of the components of the cycle, such as
proteins and metabolites, can lead to reconstruction of the cycle in the daughter cell. Self-sustaining
loops can also maintain the transcription levels of genes. For example, a transcriptional selfsustaining loop is most likely responsible for white-opaque switching in Candida albicans, a
change in phenotypic state that involves a change in cell appearance, mating behavior, and preferred
host tissues that is heritable for many generations. (2) Structural inheritance of cell structures, such
as cellular membranes and the cilia on the cell surface of ciliates. (3) Chromatin marking of various
kinds that consists of molecular marks on chromosomes (specifically, DNA methylation and histone
modifications, which involve chemical groups attached to DNA and to proteins around which the
DNA molecules are wrapped in eukaryotic cells). Some of these marks are copied by dedicated
copying machinery, others seem to be reconstructed as a result of regular genome dynamics from
partial markings transmitted to daughter cells (Henikoff, Furuyama, & Ahmad 2004). (4)
Inheritance of small RNA molecules that affect gene expression. The most well-known case
involves RNA silencing (RNAi), a post-transcriptional silencing mechanism, though more and more
classes of regulatory RNA molecules and related pathways are being identified and characterized.
Epigenetics in the broad sense refers to two kinds of inheritance. (1) Cellular epigenetic inheritance
through mitotic cells and transgenerational epigenetic inheritance through meiotic cells.
Transgenerational heredity of DNA methylation has been observed in unicellular organisms, plants,
and mammals, suggesting that transgenerational epigenetic inheritance may be more prevalent than
often suspected (Jablonka & Raz 2009). (2) Hereditary effects that by-pass the germline, for
example through early developmental inputs that lead to regeneration of previous developmental
conditions (e.g., hormonal and neural conditions) and other forms of phenotypic transmission, such
as the transmission of symbionts and parasites, e.g., gut bacteria (Jablonka & Raz 2009).
In transgenerational epigenetic transmission, alternative phenotypes can persist for several, possibly
many, generations, though their persistence may be more limited than that of genetic changes. They
may thus have evolutionary effects in addition to the role played by cellular epigenetic inheritance
in the development of multi-cellular organisms that was noted above. Generally, epigenetic
inheritance piggybacks on general developmental and physiological mechanisms of cells, and is a
by product of other physiological functions, not the result of an independent copying system that is
content neutral, though this is not their defining property; DNA methylation is a notable exception.
Epigenetic inheritance typically is holistic rather than modular in its storage and transmission (i.e.,
it is not comprised of units of information that can be changed independently of one another), and
supports a limited repertoire of hereditary variants (e.g., the steady-states of a metabolic cycle).
However, one cell may include many instances of independent self-sustaining metabolic cycles and
structurally transmitted cellular components, for example, increasing the repertoire of cellular
variations that can be inherited via these forms of inheritance. Typically, EISs (with some
exceptions, such as DNA methylation) cannot transmit unexpressed (latent) information, although
the transmission of partial factors or marks, which are not sufficient for expression, may be reliably
sufficient when additional developmental factors are added.
3.3.3 Behavioral Inheritance Systems (BISs)
Jablonka and Lamb (Jablonka 2001; Jablonka & Lamb 2005) focus on three types of behavioral
inheritance: (1) Inheritance of behavior-affecting substances. The inducing substances bias the
behavior of offspring leading to limited behavioral heredity. A paradigmatic case is the
“transmission” of food preferences from mother to offspring via molecular cues passed through the
placenta. (2) Non-imitative social learning that leads to similarity in behavior. Here, naive
organisms learn through interaction with environmental circumstances that elicit particular behavior
and by observing the behavior of experienced adults, though not by copying or imitating their
behavior. A famous case of non-imitative social learning involved the spread of milk-bottle opening
behavior in blue tits and great tits. It appears that the behavior spread through the contact of birds
with open milk-bottles or with experienced birds using bottles as food sources, not by imitating the
method of opening the bottles. (3) Imitation and instruction. In contrast with the other behavioral
inheritance systems, imitation is modular (behavioral patterns are imitated independently of other
patterns in the same behavioral sequence) and may depend on a dedicated copying system or
systems.
While the GIS and EISs transmit information mostly from parent to offspring (i.e., vertically), all
behavioral inheritance systems are directly or indirectly influenced by the social environment, and
are thus capable of transmitting information to neighbors as well, that is horizontally. A second
property shared by behavioral forms of inheritance is that for a behavior to be transmitted it has to
be expressed.
3.3.4 The Symbolic Inheritance System (SIS)
The symbolic inheritance system refers to all symbolic communication, but mainly to linguistic
communication, and is unique to humans. The symbolic inheritance system shares some properties
with the genetic inheritance system, notably modularity, unlimited variability, the use of coded
information, and the capacity to transmit latent information. Its origins are in behavioral inheritance
and it shares some of the properties of behavioral inheritance, in particular the capacity for
horizontal transmission and developmental filtering of variation prior to transmission.
Jablonka and Lamb's account of cultural evolution in humans appeals to the properties of symbolic
inheritance, most critically that variations are not blindly copied but rather reconstructed by learners
in ways that are sensitive to meaning, social context, and the history of the individuals involved
(Jablonka & Lamb 2005). They contrast their view with the meme based account of cultural
evolution presented by Dawkins and Blackmore (e.g., Blackmore 1999), and argue that focusing on
replication and selection rather than on the generation of variants and on reconstruction processes is
particularly harmful for understanding cultural evolution.
3.4 Niche Construction Theory and Ecological Inheritance
Niche construction theory (Odling-Smee, Laland, & Feldman 2003) espouses the notion of
ecological inheritance through which previous generations as well as current neighbors can affect
organisms by altering the external environment or niche that they experience. This purportedly
creates an inheritance channel that operates in parallel with genetic inheritance. Ecological
inheritance is defined as the inheritance of selection pressures that were modified by niche
construction activities (Odling-Smee 2010, p. 176). Niche construction leads to ecological
inheritance if changes to the ecological niche persist or accumulate and establish modified selection
pressures. Note that while the notion of ecological inheritance suggests viewing niche construction
as a transmission process, the focus on the modifications done to the niche highlights persistence.
Extending the notion of ecological inheritance to the realm of development, Odling-Smee (2010, p.
181) defines niche inheritance as the inheritance of an initial organism-environment relationship, or
“niche,” from ancestors. Niche inheritance can thus affect organisms' development directly, rather
than through selection.
Odling-Smee et al. (2003) note that ecological inheritance “more closely resembles the inheritance
of territory or property than it does the inheritance of genes.” In particular, it includes transmission
of material resources that are difficult to construe as informational. Odling-Smee (2010, p. 181)
enumerates fundamental differences between ecological inheritance and genetic inheritance: (1)
Ecological inheritance is transmitted through an external environment. It is not transmitted by
reproduction. (2) Ecological inheritance need not depend on the transmission of discrete replicators
(though this mechanism is not ruled out). (3) Ecological inheritance is continuously transmitted by
multiple organisms, to multiple other organisms, within and between generations, throughout the
lifetime of organisms. (4) Ecological inheritance is not always transmitted by genetic relatives. It
should be noted that some of these properties of ecological inheritance are shared by extra-genetic
inheritance more generally.
Odling-Smee (2010) distinguishes two transmission channels: transmission through direct
connection during reproduction between the internal environments of parent and offspring and
transmission through an external environment. In channel 1, the internal environment, Odling-Smee
includes Jablonka's and Lamb's genetic and epigenetic inheritance systems, and some kinds of
maternal effects. In channel 2, transmission through an external environment, he includes the
inheritance of modified selection pressures in the external environments of organisms as a
consequence of prior communicative niche construction, and includes Jablonka's and Lamb's
behavioral and symbolic inheritance systems. All the inheritance systems just mentioned transmit
semantic information, according to Odling-Smee. In addition, both transmission channels are used
to transmit energy and matter. Cytoplasmatic inheritance of various kinds, and some kinds of
maternal effects, are considered by Odling-Smee to be energy and material resources transmitted
through the internal environment, and traditional ecological inheritance of selection pressures is
non-semantic inheritance that is passed through an external environment.
4. Developmental and Evolutionary Implications
One of the best arguments for studying heredity through the perspective afforded by multiple
inheritance systems is that this perspective opens up questions about the evolutionary and
developmental relations and interactions between the various inheritance systems that are
characterized. Among these questions are questions about whether each system creates new targets
of selection, about the ways in which inheritance systems may provide developmental scaffolding
for other inheritance systems, about the regulatory role they may have in relation to one another,
and about the evolution of inheritance systems. We now turn to these issues.
At the most obvious level, it is clear that non-genetic inheritance can have an effect on the
ecological conditions an organism faces by affecting or determining behavior and activities, thus
increasing or dampening selection. The result is a feedback loop between actions of the organism
and selection that leads to what Conrad Waddington referred to as the cybernetic nature of
evolution (Waddington 1961). Behavioral and symbolic inheritance, in particular, can reinforce this
process. By thus affecting the selective challenges faced by the organism, the evolutionary feedback
loop can turn short-term hereditary effects, that would not survive many generations, into long term
evolutionary change. Section 4.4 further discusses the ramifications of this phenomenon.
Jablonka and Lamb (2005) present a general account of biological evolution based on the multiple
inheritance systems perspective. They argue that evolution can occur through any of the inheritance
systems they identify (e.g., the behavioral) without necessarily involving genetic changes. This can
happen through natural selection operating on non-genetic hereditary variations. Epigenetic changes
are usually generated at a higher rate than genetic changes, often as a result of changes in
environmental conditions, and the variation that is generated may have a higher chance of being
beneficial than blind variation. This may allow rapid adaptation to changing conditions. These
claims apply to behavioral inheritance and symbolic inheritance as well. Shea, Pen, & Uller (2011)
distinguish between adaptation resulting from selection on epigenetic variations, which they term
selection-based effects, and the adaptation resulting from induced response to the environment,
which they term detection-based effects, and discuss their evolutionary and developmental
consequences. Selection-based effects lead to adaptation via natural selection operating on reliably
transmitted epigenetic variations and are analogous to the selection-based effects of genetic
inheritance, though epigenetic variation may occur more rapidly and its frequency may increase due
to environmental challenges. Detection-based effects, in contrast, are the result of directional
variation and are a form of phenotypic plasticity.
While Jablonka's and Lamb's approach is similar to that of Maynard-Smith & Szathmáry (MaynardSmith & Szathmáry 1995), in that Maynard Smith and Szathmáry focus on changes in the way
hereditary information is stored and transmitted, Jablonka and Lamb argue that Maynard Smith and
Szathmáry neglect the evolutionary role played by distinct information-transmitting systems. In
particular, they argue that Maynard Smith and Szathmáry's approach neglects the role of instructive
processes, of the sort typically found in EISs, BISs, and the SIS, which lead to induced hereditary
changes that are acted upon by natural selection (Jablonka & Lamb 2005, p. 343). Maynard Smith
and Szathmáry, in contrast, argue that even with the existence of epigenetic inheritance processes,
natural selection working on mutations that are typically not adaptive (i.e., non-directed) remains
the fundamental evolutionary process (Maynard-Smith & Szathmáry 1995, p. 249).
4.1 Units of Selection
Once it is accepted that more than one inheritance system or, alternatively, more than one replicator
may be involved in the reproduction of organisms (let alone multiple kinds of replicators), questions
about units of selection have to be addressed. As each inheritance system can lead to hereditary
variations, there may be multiple lineages related to the production of a single organism and even
single phenotypic traits. Evolution may happen in each lineage, and, in particular, each lineage may
be “tracked” by natural selection.
According to the traditional view in evolutionary theory selection operates on individual organisms.
This view can incorporate multiple inheritance systems and channels within a single evolutionary
process by viewing each inheritance system or channel as providing developmental resources for
the construction of individual organisms, leading to a single evolutionary process operating on
lineages of organisms. Alternatively, lineages of phenotypic traits that may be affected by more
than one inheritance system or channel may be subject to selection. According to this view
phenotypic traits are the targets or units of selection (Jablonka 2004).
According to views that explain evolution in terms of replicators, multiple kinds of replicators can
support multiple and distinct evolutionary processes. The most prominent example of this line of
thought concerns the view that genes are supplemented by memes that are units of cultural
transmission, and each is manifested in a separate evolutionary process: biological evolution
operating on lineages of genes and cultural evolution operating on lineages of memes. The extended
replicator framework, in contrast, accepts the possibility of multiple kinds of replicators, but
considers a single evolutionary process that determines the fate of lineages of different kinds of
replicators by the success of their associated interactors and extended phenotypic effects (Sterelny
et al. 1996, p. 378).
4.2 Scaffolding
William Wimsatt and James Griesemer (2007) discuss multi-channel inheritance using the notion of
scaffolding from developmental psychology. Scaffolding refers to structures and functional
processes that provide a supporting framework for development. Traits inherited through one
inheritance system can provide scaffolding for other inheritance systems. Wimsatt and Griesemer
suggest that if the flow of information must be scaffolded in such a way that carriers develop in
appropriate conditions in order to assimilate, use, and carry the information, then the scaffolding
must propagate or persist alongside the information in the channel — leading to multi-channel
inheritance (Wimsatt & Griesemer 2007, p. 286). They suggest that this applies to any information
that is sufficiently complex. As a consequence it applies essentially to all biological and cultural
phenomena.
A related notion is suggested by Peter Godfrey-Smith, who defines scaffolded reproducers as
“entities which get reproduced as part of the reproduction of some larger unit (a simple reproducer),
or that are reproduced by some other entity” (Godfrey-Smith 2009, p. 88). This notion is more
restricted than Wimsatt's and Griesemer's appeal to scaffolding, as it only refers to scaffolding of
reproduction. Godfrey-Smith classifies genes as scaffolded reproducers since they rely on cellular
machinery for their reproduction (p. 130).
4.3 The ontogeny of inheritance systems
Inheritance system themselves develop so as to be able to store, transmit, and receive hereditary
information. Put differently, the inheritance of the capacity for inheritance may itself involve
developmental reconstruction processes. These developmental processes may depend on two types
of resources: resources and cues from other inheritance channels (e.g., the genetic system specifies
elements of the brain, which are required for behavioral inheritance), and cues that are transmitted
through the same channel and affect its further development (e.g., linguistic cues affecting linguistic
abilities).
An interesting example from recent research is the suggestion that sensorimotor experience plays a
role in the development of the capacity for imitation in the human brain (Catmur, Walsh, & Heyes
2009). It is argued that if this model is correct, then “human imitation is not only a channel, but also
a product of cultural inheritance” (Catmur et al. 2009, p. 2376), since imitation not only takes part
in cultural inheritance, it is shaped by it as well. Thus, cultural inheritance may provide scaffolding
for the development of imitation abilities in humans, which further affect behavioral and cultural
inheritance.
4.4 Assimilation
One of the most interesting ways in which multiple inheritance systems can interact evolutionarily
is through processes such as the Baldwin Effect and genetic assimilation. These notions purport to
explain how selection can drive developmental responses to environmental demands to become less
dependent on the presence of the external stimuli, and become increasingly hereditary. In these
processes, non-genetic variants affect the selection of genetic variations in favor of those that
produce congruent phenotypic results (Jablonka & Lamb 2005, chap. 7). In the simplest case,
originally discussed by Baldwin, a developmental response to the environment allows organisms to
survive and reproduce for enough generations for genetic mutations to accumulate through natural
selection and make the developmental accommodation to the external stimulus unnecessary. The
genetic mutations that are favored are those that act in tandem with the developmental response.
Conrad Waddington characterized a process he termed genetic assimilation leading to similar
results, but emphasized the role played by changes in combinations of genes and reorganization of
genetic networks following the reshuffling of genes during the sexual process.
Both processes involve evolution of the capacity of the organism to developmentally respond in an
appropriate way. The result of such processes is that the induced developmental response affects the
subsequent evolutionary trajectory of the lineage. The developmentally produced variants that lead
the assimilation process need not be hereditary, and may be the result of recurrent plastic
developmental responses in each generation. When they are hereditary, however, their inheritance
can reinforce their spread in the population.
A similar phenomenon can result from processes of niche construction, which affect the selective
environment faced by organisms and their descendants (Odling-Smee et al. 2003). A particularly
well known example of the possible effects of cultural niche construction on genetic evolution is the
relationship between a history of dairy farming in a culture and the prevalence of adults with a
genetic variant enabling them to continuously produce lactase, the enzyme needed to digest fresh
milk (Durham 1991; Mace 2009). This example illustrates how cultural evolution can drive genetic
evolution.
Phenomena such as these may be characterized as being “Lamarckian” in flavor, even though they
operate according to traditional Darwinian theory, since they provide room for instructive or
induced processes in evolution. The epigenetic, behavioral, and symbolic dimensions in evolution
discussed by Jablonka and Lamb produce induced variation which may affect evolution through
processes of assimilation as well as through their hereditary affects. In this way various inheritance
systems other than the genetic can indirectly affect the evolution of genetic traits.
Assimilation may typically result in the response being partially rather than entirely independent of
external stimuli. In other words, the response may become less dependent on external stimuli, and
more biased in favor of particular results, without becoming automatic. Jablonka and Lamb call this
phenomenon partial assimilation (Jablonka & Lamb 2005, p. 290), and see it as particularly
important for understanding the way behavior (BISs) and language (the SIS) affect the evolution of
mind. A further mechanism, identified by Avital and Jablonka, is assimilate and stretch. Here,
given a limited and fixed capacity for learning, new learned elements may be recruited, when part
of a behavioral sequence that formerly depended on learning becomes genetically assimilated
(Avital & Jablonka 2000).
Alexander Badyaev suggests an evolutionary continuum of inheritance systems that reflect the
extent or stage of assimilation from epigenetic (in the broad sense of Jablonka and Lamb) to genetic
inheritance. Parental effects may be a transient stage along this continuum, whose assimilation
depends on the dynamics of the environment, and other constraints (Badyaev 2009; Badyaev &
Uller 2009; Helanterä & Uller 2010).
The overall picture that emerges from the consideration of assimilation is of evolution driven by
developmental capacities and biases that affect which genetic mutations are selected. Mary-Jane
West-Eberhard summarized this observation with the claim that genes are typically followers in
evolution rather than the ones leading the way (Jablonka 2006; West-Eberhard 2003).
4.5 Regulation and control
Already in 1958 David Nanney suggested that the difference between genetic and what we would
now call cellular epigenetic inheritance lies not in their physical location (i.e., whether they lie in
the nucleus or the cytoplasm), but rather that the genetic system maintains a set of “library
specifications” while the epigenetic control system (to use his terminology) determines which
specificities are expressed in each particular cell, accounting for cell differentiation (Nanney 1958).
The epigenetic inheritance system thus plays a regulatory role in relation to the genetic system.
Considering epigenetic control systems as providing a regulatory function allowed Nanney to
suggest that they may be expected to be (1) less stable, (2) more susceptible to extrinsic control than
genetic systems, and (3) exhibit a limited number of “states”, since they are constrained by the
information available in the genetic system at each particular time (Nanney 1958). These properties
are indeed exhibited by the cellular epigenetic systems that have since been identified, which play a
role in cellular (e.g., genomic) regulation. DNA methylation and histone modifications can lead to
gene silencing, for example. The transgenerational hereditary properties of epigenetic markings
may be subsequent to their regulatory function; however, in multicellular organisms,
transgenerational heredity of epigenetic marks is constrained by their developmental role, since
parental epigenetic markings may have to be reset in gametes so that they can fulfill their
developmental function anew in offspring (Shea et al. 2011).
4.6 Evolution of Inheritance Systems
Various suggestions have been made about the evolutionary history underlying the multiple systems
of inheritance that have been identified and about their role in the evolution of life. In general,
epigenetic inheritance allows rapid response to inducing stimuli and may be more advantageous
than mutation/selection cycles in specific types of fluctuating environments. This may be
particularly important in small populations and diploid organisms, in which mutations are typically
recessive (Nanney 1960). Maynard Smith and Szathmáry argued that evolution typically moves
from limited to unlimited systems of inheritance or, to use their conceptual framework, from limited
to unlimited hereditary replicators, and from holistic to modular replication (Maynard-Smith &
Szathmáry 1995; Szathmáry 2000). This evolutionary trend is manifested in the major transitions in
evolution to new levels of individuality (and new kinds of inheritance) that they have characterized.
However, the co-existence of multiple systems of inheritance and its evolutionary significance is
downplayed by such an account. Jablonka and Lamb (Jablonka 1994; Jablonka & Lamb 2006), in
contrast, emphasize the role played by inheritance systems other than the genetic, in particular by
epigenetic inheritance, in evolutionary transitions. They place particular importance on the role of
epigenetic inheritance in the evolution of multi-cellularity (see also Maynard-Smith 1990; Nanney
1958, 1960; Shea et al. 2011) and in the evolution of the chromosome (Jablonka & Lamb 2006).
Nanney (1960) suggested that epigenetic inheritance played a role in cell specialization in
unicellular populations (colonies), which conferred economic benefits to individual cells and
enabled populations to survive environmental traumas due to their heterogeneity, prior to the
emergence of true multi-cellularity. In addition, Jablonka (Jablonka 2001, p. 113) argues that with
the evolution of repair and compensatory mechanisms inheritance systems become more limited.
Two ways around the evolutionary stasis that would result are the move to higher levels of
individuality (Jablonka 1994), and the transition to coded information. Ruth Sager (1966) suggested
it may be adaptive to use inheritance systems minimizing variability to control traits that are crucial
for survival.
Kim Sterelny (2001) presented a set of requirements that an inheritance system (“replication
system,” in his words) should meet if it is to support evolvability. Three fundamental properties are
necessary: (1) blocking outlaws; (2) stable transmission of phenotypes; (3) generation of variation.
Using these high-level desiderata, Sterelny articulates a series of nine conditions, called the Hoyleconditions after Sterelny's thought experiment: a vertical, i.e., “only to offspring and from parents”
(C1), simultaneous (C2), and unbiased transmission (C3) of components (or replicators) that are
irreversibly committed to their biological role as replicators (C4). Further, to ensure stability,
replication has to be high-fidelity (C5), and the mapping between replicators and system
organization (i.e, “the genotype-phenotype map”) has to be robust (C6). The requirement to support
the generation of variation is cashed out in terms of being able to support a large, if not unlimited,
set of variants or, in Sterelny's framework, replicators (C7), having a “smooth” (quasi-continuous)
mapping between replicators and system organization, i.e., small changes should result in small
effects on organization (C8). Finally, the generation of biological organization from replicators
should be modular (C9), in the sense that each replicator or small group of replicators should be
responsible for only one or a few traits. Whether an inheritance system fulfills the Hoyle conditions
is a matter of degree. Clearly, the genetic system comes closest to meeting the full set of Hoyle
conditions. Responding to Sterelny's arguments, Griesemer et al. argue that we should direct our
attention to the evolution of inheritance systems (Griesemer et al. 2005). They note that the Hoyle
conditions are a product of evolution, not a necessary precondition for inheritance that can support
evolvability. In addition, they point out that the Hoyle conditions may be met in a distributed
manner, that is by multiple inheritance systems each of which fails to meet the criteria on its own
but that together give rise to the required properties. Griesemer et al. also argue that the Hoyle
conditions may conflict: satisfying one may limit the ability to satisfy others.
A significant aspect of the evolution of inheritance systems that is neglected by most contemporary
accounts is the relationship between properties of populations and fine-grained properties of
inheritance systems, in particular the relationship between the properties of inheritance systems and
the mating strategies of species. The phenotypic variations produced by an inheritance system
depend on population level considerations such as these which determine, for example, the
frequency of heterozygotes (and hence the significance of dominance and recessivity) and the
probability that calibrated gene networks will not be disrupted by sexual reproduction (e.g., because
genes are adjacent on the chromosome or because the alleles are fixed in the relevant population).
Population-level considerations also apply to the analysis of epigenetic variation and inheritance.
For example, population size may affect the evolutionary consequences of induced epigenetic
variation (Rapp & Wendel 2005). Population level considerations are not typically addressed by
contemporary accounts of inheritance systems, yet clearly have evolutionary implications.
This issue was central to Cyril Darlington's analysis in his 1939 book The Evolution of Genetic
Systems (Darlington 1939). Darlington noted that the organization of the karyotype, or the “genetic
system” to use his terminology, and its dynamics throughout the mating group, affect the hereditary
combinations that are produced, and hence hereditary variation, and can lead to reproductive
isolation and speciation. The following quote gives the general flavor of Darlington's line of
thought,
There must be a relationship between the hereditary materials, and their behaviour, throughout the
whole group or species; and it is on this relationship the genetic system depends for its character.
Hybridity optimum, segregation, and recombination must all be related throughout the group.
Furthermore, they must be related not merely amongst themselves, but also to the mating habits of
the individuals which compose the group, and to the barriers which make that group by separating
or isolating it from others. (Darlington and Mather 1949, 237; their italics).
Darlington argued that the genetic system of a species is connected to its preference for inbreeding
or outbreeding, since together they affect the frequency of heterozygosity (Darlington 1939;
Darlington & Mather 1949). He noted that Mendelian inheritance establishes a cycle between free
and potential (latent) genetic variability (Darlington & Mather 1949, p. 276): Potential variability is
contained by heterozygotes, while free variability is exhibited by the phenotypes of their offspring
as a result of segregation.
5. Conclusions
The study of inheritance systems combines attention to the growing knowledge about inheritance
mechanisms and processes in nature with reflection about the nature and dynamics of the
evolutionary process. The term “inheritance system” is typically used to refer to mechanisms and
factors involved in inheritance, but the term lacks a standard definition which goes beyond
enumerating various purported inheritance systems, and it is unclear if a single definition can
capture the different uses of the term. A principled definition that determines how inheritance
systems are individuated and delimited may be essential for addressing many conceptual issues that
remain open (see Griesemer et al. 2005). The lack of a universally accepted definition may explain
the fruitfulness of the term but also suggests caution.
The discussion above tried to present a unified framework for the discussion of inheritance systems
that is not tied to any particular account. It contrasted the multiple inheritance systems view with
monist (e.g., geno-centrism) and holistic views (e.g., DST) about inheritance (section 1.2) and
stressed the developmental, mechanism-oriented, perspective on reproduction that underlies many
discussions of inheritance systems (see section 2).
The multiple inheritance system perspective highlights a variety of questions (see section 4) and
many fundamental questions remain open. Some of them depend on empirical work, perhaps most
importantly determining the prevalence and stability of transgenerational epigenetic inheritance
(Helanterä & Uller 2010; Jablonka & Raz 2009; Shea et al. 2011). The developmental aspects of
many of the inheritance systems discussed in this entry, in particular behavioral inheritance, are still
not fully understood. Generally, many open questions remain about the interactions between the
various systems and about their evolution, in particular the evolution of social learning and the
evolution of language. A crucial element downplayed by most contemporary accounts is the
connection between population level issues, such as population size, mating strategies, etc., and the
properties of inheritance systems. Addressing these issues requires quantitative modeling, and
eventually the integration of multiple inheritance systems with their different characteristics into
population genetics.
Non-genetic inheritance can have short term evolutionary effects and can affect genetic evolution
(e.g., through genetic assimilation). However, the long-term and macro-evolutionary significance of
non-genetic inheritance, and in particular its effects on the way populations respond to selection is
still being debated (e.g., Helanterä & Uller 2010, p. 4). Jablonka's and Lamb's evolutionary views
stress the role of “soft inheritance,” or the inheritance of acquired characters, which is exhibited by
many of the non-genetic inheritance systems. Partly on account of this they are among those who
raise the need to revise and extend the Modern Evolutionary Synthesis (Pigliucci & Müller 2010).
The Modern Synthesis marginalized soft inheritance and viewed significant evolutionary change to
be solely the result of gradual selection working on random variations. The assumptions underlying
this view are challenged by work on non-genetic inheritance.
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Other Internet Resources

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Tetrahymena Biogeography, David L. Nanney's archive of historical and autobiographical
texts about epigenetic inheritance in Tetrahymena.
Epigenomics, Links to resources on epigenetics and epigenomics, from U.S. Department of
Health and Human Services, National Library of Medicine.
Related Entries
evolution: cultural | heritability | information: biological | replication and reproduction
Copyright © 2012 by
Ehud Lamm <[email protected]>