## 1. Introduction


### 1.1 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.


### 1.2 Early Work On Non-Genetic Inheritance



Modern evolutionary theory equates inheritance with the transmission
of genes from parents to offspring and as such focuses only on genetic
inheritance (which will be further described in section 3.3.1).
Nevertheless, 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, non-Mendelian 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. Although the distinction
between these two groups of questions is useful, many of the topics
and controversies to be discussed in this entry involve both.


### 1.3 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 and Reproduction),
 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 dual-inheritance 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 (for detailed discussion of the notion of
cultural inheritance see the entry on
 cultural evolution).
 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 Eors Szathmary's 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 & Szathmary 1995), and multiple
types of replicators are embraced by the notion of the extended
replicator (Sterelny 2001; Sterelny et al. 1996, see entry:
 Replication and Reproduction)
 discussed below. More typically, however, non-genetic forms of
inheritance, with the possible 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 (regarding
the debate whether human cultural evolution is best understood through
applying a replicator framework to learning and imitation, see Lewens
2015, chps. 1 and 2). 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 very 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
acting on variation in 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 extra-genetic 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, 2005/2014,
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 non-genetic 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). In more
recent work, Griffiths appeals to causal specificity for roughly the
same purpose. He frames the debate as being about the extent to which
non-genetic inheritance is involved in the precise determination of
the phenotype, or how specific the causal relation is (see
 section 2.4).


### 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: 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 multi-cellular 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 (see 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: S361, 2000b, 2000c, see
also the entry on
 replication,
 section 8). 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: 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: 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 case 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: 364). According to Griesemer's classification, epigenetic
inheritance processes can be classified as inheritance processes which
are not replication processes (Griesemer 2000c: 250).



Both Griesemer and Godfrey-Smith applied their respective notions of
reproducers to the question of collective reproduction, involving
entities that can reproduce but that contain other things than can
also reproduce (see Godfrey-Smith 2012, Griesemer 2018; for further
discussion see entry on
 the biological notion of individual).
 The paradigmatic test cases are multi-cellular organisms (arguably,
collective reproducers) and animal groups (who are arguably not).
Griesemer focuses on the role of scaffolding and levels of
compositional organization, while Godfrey-Smith characterizes
collective reproduction according to the degree of overall integration
of the reproducer, the degree of reproductive (germ/soma)
specialization, and the degree of a reproductive bottleneck. The
properties characterizing collective reproducers are arguably related
to the inheritance systems involved (for one intriguing suggestion
concerned with the role of epigenetic inheritance in the origin of the
germ-line see Lachmann & Libby 2016). 



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 2005/2014) 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 to 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: 334, see also the discussion in Sterelny et al. 1996: 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). In recent work Griffiths applies an
information-theoretic measure of causal specificity to measure how a
given factor contributes to the precise determination of the
phenotype. This measure is produced by combining the classic notion of
mutual information, as found in Shannon information theory, with
Woodward's notion of speficity of causes (Woodward 2010).
Griffiths (2017) argues that this framework naturally extends to
various epigenetic marks and non-coding regions of DNA that are
causally specific, while at the same time distinguishing these cases
from many other causes of the same outcomes, such as the presence of
RNA polymerase, that lack such specificity.



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 Sterelny 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 types
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



An important distinction between *inheritance channels* and
*inheritance systems* should be made before classifying
inheritance systems. This distinction plays a central role in
controversies over classifying and delimiting inheritance systems.
Simply put, inheritance channels refer to "routes across
generations" (in the words of Sterelny et al. (Sterelny et al.
1996: 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 used in multiple inheritance
channels. 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:. 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. For example, DNA methylation, an epigenetic mark, copied in
cellular epigentic inheritance, is tied to the copying and
transmission of DNA. This arguably constitutes a single channel.
Epigenetic mechanisms and heredity play a role in various properties
of the genetic system, affecting things such as mutation and
recombination rates and hence genetic variation. Perhaps more
fundamentally, epigenetic mechanisms are part of the mechanisms
'operating' the genetic channel. The inheritance of the
genome, when a cell divides, involves recreation of the mother
cell's epigenetic state, a process that goes beyond copying
(Lamm 2011, 2014; Lamm & Jablonka 2008).



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. DST proponents argue that some
developmental resources are not easily represented as channels,
especially persistent resources, that holism is more heuristically
productive, and that channels are not statistically independent
information carriers (Griffiths & Gray 2001; see also the useful
discussion by Griesemer et al. (2005: 526)).



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 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, 2005/2014). 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: 100; Jablonka &
Lamb 2005/2014). 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 mechanismic 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 & Szathmary 1995: 43), and the ability to generate
fine-grained response to selection (see Griffiths 2001: 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 Mechanismic 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.



Jablonka and Lamb's classification of inheritance systems on the
basis of their mechanismic differences is not the only classification
approach which focuses on hereditary variations. Recently,
Helantera & Uller (2010) analyzed the inheritance systems
Jablonka and Lamb identified based on their evolutionary consequences.
They claim that Jablonka 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. Similarly, Day and
Bonduriansky (2011), using a unified framework based on the Price
Equation, have argued that while the diversity of inheritance
mechanisms is very large they give rise to a much more limited set of
inheritance *patterns*, characterized as unique combinations of
reproductive transmission rules.



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: 100).
In more recent work Jablonka and Lamb (2005/2014) 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.





|  |  |  |  |  |  |
| --- | --- | --- | --- | --- | --- |
| Inheritance system | Organizations of information | Dedicated copying system? | Transmits latent (nonexpressed) information? | Directions of transmission | Range of variation |
| Genetic | Modular | Yes | Yes | Mostly vertical | Unlimited |
| Epigenetic |  |
| *Self-sustaining loops* | Holistic | No | No | Mostly vertical | Limited at the loop level, unlimited at the cell level |
| *Structural templating* | Holistic | No | No | Mostly vertical | Limited at the structure level, unlimited at the cell level |
| *RNA silencing* | Holistic | Yes | Sometimes | Vertical and sometimes horizontal | Limited at the single transcript level, unlimited at the cell
level |
| *Chromatin marks* | Modular and holistic | Yes (for methylation) | Sometimes | Vertical | Unlimited |
| *Organism-level developmental legacies* | Holistic | No | No | Mostly vertical | Limited |
| Behavioral |  |
| *Behavior-affecting substances* | Holistic | No | No | Both vertical and horizontal | Limited at the single behavior level, unlimited for
lifestyles |
| *Nonimitative social learning* | Holistic | No | No | Both vertical and horizontal | Limited at the single behavior level, unlimited for
lifestyles |
| *Imitation* | Modular | Probably | No | Both vertical and horizontal | Unlimited |
| Symbolic | Modular and holistic | Yes, several | Yes | Both vertical and horizontal | Unlimited |



Table 1. The reproduction of
information



  




|  |  |  |  |  |
| --- | --- | --- | --- | --- |
| Inheritance system | Variation is targeted (biased generation)? | Variation subject to developmental filtering and
modification? | Variation constructed through direct planning? | Variation can change the selective environment? |
| Genetic | Generally not, except for the directed changes that are part of
development and the various types of interpretive mutation | Usually not, although expressed genetic changes may have to
survive selection between cells prior to sexual or asexual
reproduction | No | Only insofar as genes can affect all aspects of epigenetics,
behavior, and culture |
| Epigenetic | Yes, a lot of epigenetic variations are produced as specific
responses to inducing signals  | Yes, selection can occur between cells prior to reproduction;
epigenetic states can be modified or reversed during meiosis and early
embryogenesis | No | Yes, because the products of cellular activities can affect the
environment in which a cell, its neighbors, and its descendants
live |
| Behavioral | Yes, because of emotional, cognitive, and perceptual biases | Yes, behavior is selected and modified during the animal's
lifetime | No | Yes, new social behavior and traditions alter the social and
sometimes also the physical conditions in which an animal lives |
| Symbolic | Yes, because of emotional, cognitive, and perceptual biases | Yes, at many levels, in many ways | Yes, at many levels, in many ways | Yes, very extensively, by affecting many aspects of the social
and physical conditions of life |



Table 2. Targeting, constructing, and
planning transmitted variation




(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*, 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 (Szathmary 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,
2014).



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 (2005/2014): (1) Self-sustaining 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
self-sustaining 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 (e.g., Henikoff, Furuyama,
& Ahmad 2004; reviewed in Lamm 2014). (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; 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
2005/2014). They contrast their view with the meme based account of
cultural evolution presented by Dawkins and Blackmore (e.g., Blackmore
1999), which takes cultural items to be stored in human brains and
transmitted to other human agents in the form of faithful replication,
and cultural change to involve the differential success of replication
of the different cultural items. Jablonka and Lamb 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: 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:
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. For a recent
discussion of the differences between selective niche construction and
developmental niche construction see Stotz (2017).



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: 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. Cytoplasmic 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.



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 (2005/2014) 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 the
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 & Szathmary (Maynard Smith &
Szathmary 1995), in that Maynard Smith and Szathmary
focus on changes in the way hereditary information is stored and
transmitted, Jablonka and Lamb argue that Maynard Smith and
Szathmary neglect the evolutionary role played by distinct
information-transmitting systems. In particular, they argue that
Maynard Smith and Szathmary'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: 343). Maynard
Smith and Szathmary, 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 & Szathmary 1995: 249).


### 4.1 Units of Selection



Once it is accepted that more than one inheritance system or,
alternatively, more than one independently inherited 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 (qua interactors). 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: 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 (see Caporael et al. 2013). 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: 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: 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 systems 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).
Recent research on chromatin dynamics makes it clear that genetic
inheritance relies on multiple epigenetic mechanisms, and suggests
that we should be cautious with the distinction between a genetic
inheritance system and cellular epigenetic inheritance systems (Lamm
2011, 2014).



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: 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
(see Ancel 1999, 2000; Crispo 2007; Scheiner 2014, Weber & Depew
2003). In these processes, non-genetic variants affect the selection
of genetic variations in favor of those that produce congruent
phenotypic results (Jablonka & Lamb 2005/2014: 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. 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, a
element of gene-culture coevolution.



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: 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; Helantera & Uller 2010; see also: Yona et al.
2015).



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). Thus, according to Nanney, the
epigenetic inheritance system 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 (1) be
less stable, (2) be 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; see also Lachmann & Libby 2016).


### 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 Szathmary
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 & Szathmary 1995;
Szathmary 2000, 2015). 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: 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 Hoyle-conditions 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, in the
genetic case, 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: 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 attempts to synthesize recent
discoveries about inheritance mechanisms and processes in nature with
reflection about the nature and dynamics of evolutionary processes.
The term "inheritance system" is typically used to refer
to both 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--if indeed they can be-- 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 approaching the
literature with caution.



The discussion above tried as much as possible 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 (i.e., geno-centrism) and holistic views
(i.e., DST) about inheritance
 (section 1.3)
 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
(Helantera & 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 (see Day & Bonduriansky 2011, Geoghegan &
Spencer 2012).



Several topics that are receiving significant attention in the biology
research community are directly related to the discussion of
inheritance systems. One is the invigorated field of cultural
evolution and social learning (see Whiten 2017). A second area is the
discussion of inheritance of regulatory RNA molecules, an epigenetic
inheritance process that goes beyond the transmission of RNA and
involves developmental re-production (see Veigl 2017). A third area,
already receiving significant attention from philosophers, is the
hereditary properties and function of the microbiome. This is tied to
the recent interest in holobionts, a term that refers to assemblages
of multiple species, notably multi-cellular organisms and bacteria,
that form ecological and potentially evolutionary units. It has been
argued by some researchers that holobionts are units of selection and
that the combined genome of the host and symbionts, dubbed 'the
hologenome', is conceptually analogous to the genome, with the
bacteria being analogous to genes. Arguably, this inheritance system
has Lamarckian dimensions. Other researchers argue that the degree of
vertical transmission of symbionts is typically too low to qualify the
holobionts as units of selection. For discussion of these issues see
Hurst (2017), Opstal & Bordenstein (2015), and section IV of
Gissis, Lamm & Shavit (2018). Finally, increasing knowledge of the
genetic system itself, in particular the role of chromatin shape and
dynamics in gene expression as well as in mutation, recombination, and
other fundamental processes, may lead to new perspectives on the
relation between the genetic system and epigenetic mechanisms, and
improve our understanding of the transmission of chromatin state.
Arguably, the DNA and non-DNA components of the genome should be seen
and studied as a dynamic and responsive developmental system (Lamm
2011, 2014). Moreover, better understanding of how genetic adaptation
is reached under experimental conditions suggests how physiological
and epigenetic responses may facilitate adaptation via other means,
making a fitness improving response increasingly more robust, up to
potentially becoming established via appropriate mutations (Yona et
al. 2015). These results may lead to rethinking the dichotomy between
plasticity and evolvability (Lamm & Jablonka 2008) and support the
idea of "natural genetic engineering" systems (see Shapiro
2011). 



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.,
Helantera & Uller 2010: 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 & Muller 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.