Organisms inherit various kinds of developmental information and cuesfrom their parents. The study of inheritance systems is aimed atidentifying and classifying the various mechanisms and processes ofheredity, the types of hereditary information that is passed on byeach, the functional interaction between the different systems, andthe 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, fromparents to offspring. It is, however, clear on reflection that thereare other ways in which offspring may receive from parents resourcesor cues that affect their development. This is particularly apparentin humans, and the suggestion that social and cultural cues may serveas an additional “inheritance system” has been made manytimes. These observations, and the models of dual inheritance of genesand culture (e.g., Boyd & Richerson 1985; Cavalli-Sforza &Feldman 1981; Durham 1991; for a recent overview see Mesoudi 2011,Lewens 2015), are a useful starting point from which to approach themore general project of elucidating the notion of inheritance system.Cultural inheritance, however, is a broad category, whereas theanalysis of inheritance systems discussed below tends to be morefine-grained (see Sterelny 2001: 337). The term “inheritancesystems” is used to describe different mechanisms, processes,and factors, by which different kinds of hereditary information andvariation are stored and transmitted between generations.

We present the discussion of inheritance systems in the context ofseveral debates. First, between proponents of monism about heredity(gene-centric views), holism about heredity (Developmental SystemsTheory), and those stressing the role of multiple systems ofinheritance. Second, between those analyzing inheritance solely interms of replication and transmission, and views that stress themulti-generation reproduction of phenotypic traits. A third debate isconcerned with different criteria that have been proposed foridentifying and delimiting inheritance systems. A fourth controversyrevolves around the evolutionary implications of the existence of thedifferent inheritance systems, for example the significance of the“Lamarckian” aspects of some of the inheritance systemsthat have been identified, such as epigenetic inheritance andbehavioral inheritance, as well as potentially the inheritance ofmicrobial symbionts (i.e., the microbiome) that allow the transmissionof environmentally induced characters (i.e., “softinheritance”).

This entry is organized as follows: Sections 1 and 2 provide commonground and historical context for the discussion. Section 3 discussesspecific accounts of inheritance systems. General evolutionaryimplications are presented in section 4. Finally, section 5 summarizessome of the open questions in the field.

• 1. Introduction
  • 1.1 Heredity and Inheritance
  • 1.2 Early Work On Non-Genetic Inheritance
  • 1.3 Monism, Holism, and Multiple Systems views
  • 1.4 Variation, Hereditary Variation, and Inheritance Systems
• 2. Reproduction and Replication
  • 2.1 Multi-generation reproduction of phenotypes
  • 2.2 Inheritance and replication
  • 2.3 The reproducer concept
  • 2.4 Inheritance systems and notions of information
• 3. Classification of Inheritance Systems
  • 3.1 Inheritance Channels
  • 3.2 Identifying and delimiting inheritance systems
  • 3.3 Mechanismic Classification of Inheritance Systems
  • 3.4 Niche Construction Theory and Ecological Inheritance
• 4. Developmental and Evolutionary Implications
  • 4.1 Units of Selection
  • 4.2 Scaffolding
  • 4.3 The ontogeny of inheritance systems
  • 4.4 Assimilation
  • 4.5 Regulation and control
  • 4.6 Evolution of Inheritance Systems
• 5. Conclusions
• Bibliography
• Academic Tools
• Other Internet Resources
• Related Entries

1. Introduction

1.1 Heredity and Inheritance

It is useful to distinguish between the following terms. The termsheredity andhereditary will be used henceforth torefer to reliable resemblance relations between parents and offspring.Particular traits (phenotypic or genotypic) may be hereditary in this sense.^[1] The terminheritance will be used to refer to causalprocesses of transmission between parents and offspring that accountfor heredity, and the mechanisms responsible for them. We might, forexample, say that eye color is hereditary, and that geneticinheritance accounts for the heredity of eye color (or, more formally,for the heredity of variations in eye color). Multiple inheritanceprocesses may be implicated in the heredity of a particular phenotypictrait. Inheritance is often construed as transmission of information,though this notion raises difficulties; this issue is discussed insection 2.4.

The termsparent andoffspring are used in a generalsense, since transmission may be from individuals other than thegenetic parents of the organism (i.e., non-vertical). Multipleinheritance systems may lead to multiple“parent-offspring” relations.

1.2 Early Work On Non-Genetic Inheritance

Modern evolutionary theory equates inheritance with the transmissionof genes from parents to offspring and as such focuses only on geneticinheritance (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 geneticinheritance (Jablonka & Lamb 2005; Sapp 1987). Two fundamentaltypes of arguments led to this conclusion: arguments based onobservations regarding patterns of inheritance, and argumentsconcerned with the localization of hereditary factors inside cells.Arguments of the first kind were based on hereditary relations andinheritance patterns that fail to conform to the rules of Mendelianinheritance (e.g., maternal inheritance). If Mendelian inheritancepatterns are the result of the way the chromosomes in the eukaryoticcell nucleus behave, non-Mendelian heredity must depend on separateinheritance processes, mechanisms, or systems (Beale 1966; Sager1966). Second, there were observations of hereditary phenomena thatseemed to depend on factors residing in the cytoplasm of cells, ratherthan their nucleus, where the genetic material is localized. Theinterpretation of these observations was highly contested (Darlington1944; Sapp 1987).

Today, we know that some of these observations are related to the(maternal) inheritance of organelles residing in the cytoplasm, suchas the mitochondria and chloroplasts, organelles which carry their ownDNA. This however does not encompass all the mechanisms which underliecytoplasmatic inheritance. Paradigmatic work on cytoplasmaticinheritance done by Sonneborn, Beale, Nanney, and their colleagues inthe 1950s and 1960s, was concerned with patterns of inheritance inunicellular organisms, and in particular the protist genusParamecium. It was suggested that the self-sustainingregulatory loops that maintain gene activity or inactivity in a cellwould persist through cell division, provided the non-DNA componentsof the system (many of which reside in the cytoplasm in eukaryoticmicroogranisms) were shared among daughter cells. In this way,alternative regulatory phenotypic states would be inherited. Among theproperties whose inheritance was studied were mating-type variations,serotype variations, and the structural or “surfaceinheritance” of ciliary structures. Remarkably, microsurgicalchanges to the ciliary structures on the surface ofParamecium cells are inherited by offspring. The stability ofinduced characters once the stimulus was removed (called“cellular memory”) and the number of generationscharacters were maintained varied widely. However, the resultsindicated that long-term stability and heritability need not be theresult of changes to the DNA sequence (Nanney 1958).

During the 1950s to 1970s a growing set of observations indicated thatdetermined and differentiated states of cells are transmitted in celllineages. These observations concerned studies of Drosophila imaginaldiscs by Ernst Hadorn; Briggs and King’s cloning experimentswith amphibians; Mary Lyon’s work on X-chromosome inactivation;and work establishing thein vitro clonal stability ofcultured cell lines. Eventually, the termepigeneticinheritance came to refer to hereditary variation that does notinvolve changes to the DNA sequence.

The brief account of some of the early work on unicellular organismsgiven above illustrates some of the distinctions that are elaboratedin the rest of this entry. One group of questions is concerned withthe properties of hereditary relations, the sources of variations (inparticular, whether they can be environmentally induced), thestability of variations and their regulation, and so on. A secondclass of questions is concerned with the way hereditary information isstored and transmitted. It is here that we can locate the debatesabout nuclear versus cytoplasmatic inheritance and about the primacyof DNA as the information store of the cell. Although the distinctionbetween these two groups of questions is useful, many of the topicsand 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 “mastermolecule” containing coded genetic information, after thediscovery of the double helix structure in 1953, on the one hand, andthe gene-selectionist view articulated in 1966 by George Williams inhis bookAdaptation and Natural Selection, which culminatedin 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 asconsisting of a single channel of transmission. This channel isunderstood to involve the inheritance of genetic information encodedin DNA (or, in some viruses in RNA), a view often referred to as“geno-centrism”. It should be noted that the replicatorconcept itself does not rule out non-genetic replicators (Dawkins1976, see also the discussion by Sterelny, Smith, & Dickison1996). The dual-inheritance model of biological and cultural evolutionwhich is based on two types of replicators, genes and memes, is aparadigmatic example that is based on the replicator framework, andthat involves both more than one channel of inheritance andnon-genetic inheritance (for detailed discussion of the notion ofcultural inheritance see the entry oncultural evolution). Accounts of heredity that are based on the notion of replicators mayapproach non-genetic inheritance by characterizing multiplekinds of replicators (e.g., memes), each of which is supposedto underlie a different channel of non-genetic inheritance. JohnMaynard Smith and Eörs Szathmáry’s account ofMajor Transitions in Evolution is organized aroundtransitions to new kinds of ways in which information is stored andtransmitted, understood as transitions to new kinds of replicatingentities (Maynard Smith & Szathmáry 1995), and multipletypes of replicators are embraced by the notion of the extendedreplicator (Sterelny 2001; Sterelny et al. 1996, see entry:Replication and Reproduction) discussed below. More typically, however, non-genetic forms ofinheritance, with the possible exception of cultural inheritance in afew groups of higher animals, are often ruled out as not fulfillingthe requirements imposed by the definition of a replicator (regardingthe debate whether human cultural evolution is best understood throughapplying a replicator framework to learning and imitation, see Lewens2015, chps. 1 and 2). It should be emphasized that the replicator viewposited replicators, typically genes, as the unit of selection; thework discussed in this entry is concerned with the biologicalprocesses and mechanisms involved in inheritance, and is not concerneddirectly with the debate about the unit of selection. Implicationsregarding selection are elaborated insection 4.1.

Approaches that rule out or ignore non-genetic inheritance might becharacterized as “monist” in their treatment of thequestion of the existence and significance of multiple inheritancesystems. Monist tendencies may be traced back already to WilhelmJohannsen’s work at the beginning of the 20th century. WhileJohannsen invented the term “gene” in order to remainuncommitted to a specific view about the material constitution ofhereditary factors, both this term and the notion of“genotype” that he developed suggest a monist view ofinheritance. This tendency was reinforced by molecular genetics andthe replicator framework.

How do monist views handle the other forms of inheritance that areknown to exist? Consider the mitochondria. Monist accounts regard thematernal inheritance of organelles such as the mitochondria, whichmight conceivably be thought to constitute a separate inheritancechannel, if not system, to be of marginal conceptual importance.First, it can be argued that being based on genetically codedinformation (DNA sequence), the similarities with nuclear inheritanceallows it to be seen as not involving a distinct inheritance system,if this notion is understood to refer to the way hereditaryinformation is stored and transmitted. Indeed, views that focus onmultiple inheritance systems may, for the very same reason, notconsider the inheritance of plastids as based on a distinctinheritance system. Second, it is assumed that the evolution ofcomplex organismal traits is to be explained by natural selectionacting on variation in genetic information in the nucleus. Thus,mitchondrial inheritance, and plastid inheritance more generally, areconsidered to be of limited explanatory value when trying to give ageneral account of the evolution of the organism (beyond the earlystages of endosymbiogenesis), and is of interest mainly whenconsidering the evolution of the mitochonrdia themselves, in whichcase there is yet again a single inheritance system that is relevant,that of the mitochondrial genome. Similar reasoning is applied moregenerally to reject forms of supposedly extra-genetic inheritance thatare not based on the transmission of DNA, by claiming either that theinheritance fails to be the transmission of information or that theinformation that can be transmitted is limited and thus notevolutionarily significant, and is merely the transmission of materialresources or infrastructure. Cashed out in the terms of the replicatorframework, arguments against supposed cases of extra-geneticinheritance are that they do not lead to the establishment ofreplicators, which are entities that are faithfully copied and passeddown multiple generations, yet replicators are necessary for evolutionby natural selection, or that extra-genetic inheritance leads toreplicators that are limited in the repertoire of variants theysupport (see Godfrey-Smith 2000). Proponents of the multipleinheritance systems view and of holistic views about inheritance arguethat these requirements are either unnecessary or too strong, and leadto a distorted understanding of evolution (see Griffiths & Gray2001; Jablonka 2001).

In contrast to monist views, proponents of “DevelopmentalSystems Theory” (DST) (Griffiths & Gray 1994, 2001) offer aradical reformulation of evolutionary theory, including the notion ofinheritance and the treatment of extra-genetic inheritance. DSTapplies the notion of inheritance to any developmental resource thatis reliably present in successive generations, and which is part ofthe explanation of the similarity between generations (Griffiths &Gray 2001). While embracing the existence of non-genetic inheritance,and its significance for evolutionary accounts, these researchersargue against separating these phenomena into multiple channels orsystems of inheritance (Griffiths & Gray 2001): Inheritancephenomena are so intertwined in their effects on development, and eachrelies on others to have its developmental effect, that it is bothmore realistic and scientifically more productive not to separate theminto distinct channels, systems, or replicator types. The DST approachmight be characterized as “holistic” in its treatment ofinheritance.

In contrast to monism and holism, the views discussed in this entryidentify and classify various mechanisms and processes of inheritance,the types of hereditary information that are passed on by each, thefunction and interaction of the different systems, and theevolutionary consequences of these properties. Contemporary views onevolution that stress the role of multiple systems of inheritance havebeen greatly influenced by the work Eva Jablonka and Marion Lamb, inparticular their arguments about the evolutionary role of epigeneticinheritance (Jablonka 2001, 2002; Jablonka & Lamb 1995, 2005/2014,2006) . In addition to the line of work influenced by Jablonka andLamb, extra-genetic inheritance is stressed by DST, albeit in the formof holism about inheritance, and in the “extendedreplicator” framework elaborated by Kim Sterelny et al.(Sterelny 2001; Sterelny et al. 1996).

Responding to pressure from DST, the extended replicator approachelaborates the account of non-genetic replicators provided by thereplicator framework (Dawkins 1976; Hull 1980) to include non-geneticreplicators, while retaining the replicator/interactor distinctionwhich both the holism of DST and the multiple systems view of Jablonkaand Lamb reject: Replicators form lineages, while interactors, throughwhich replicators interact with the environment, are ephemeral (seesection 2.2 for discussion). Sterelny et al. (1996) emphasize the distinctionbetween genes as factors having “a distinctive informationalrole in inheritance” and other reliably present developmentalresources. According to them, this distinctive informational roleexplains why genes, and not just any resource,represent thephenotype and have a special developmental role. They embrace othercases of biological replication if they can be informational in thestrong sense their account demands. In a nutshell, the mainrequirements are that the replicator have the biofunction (i.e.,proper function or evolutionarily selected function) of representingthe phenotype (or aspects of it) and that it play a causal role in theproduction of the phenotype. Genes according to this view do not havea unique or privileged role in determining the phenotype; however,they do have a distinctive informational role (seesection 2.4). Whether other types of replicators exist is an empirical matter, andviewing various biological processes as replication may bescientifically productive according to Sterelny et al. (1996). In morerecent work, Griffiths appeals to causal specificity for roughly thesame purpose. He frames the debate as being about the extent to whichnon-genetic inheritance is involved in the precise determination ofthe phenotype, or how specific the causal relation is (seesection 2.4).

1.4 Variation, Hereditary Variation, and Inheritance Systems

A fundamental requirement for evolutionary change via naturalselection is the existence ofvariation in the population.However, for variations to have evolutionary effect they need to be(at least partly) hereditary or heritable (see entry onheritability; I will here focus on hereditary variations and hereditarytransmissibility as defined above, and will not discuss the notion ofheritability which is a population term). It ishereditaryvariations that fuel evolution through natural selection(Lewontin 1970, 1985). Thus, if we aim to give a general account ofpossible evolutionary change we may start by examining and classifyinghereditary variations (Jablonka & Lamb 2005). Hereditaryvariation, in turn, may be accounted for in terms of inheritancemechanisms, hence by accounts ofinheritance systems. As astarting point we can understand the notion of inheritance system asreferring to mechanisms, processes, and participating factors, thatare involved in transmission between parents and offspring leading tohereditary relations. Several influential accounts of inheritancesystems that are of philosophical interest are discussed insection 3.

2. Reproduction and Replication

Work on inheritance systems is often situated in the context ofdevelopmental evolutionary biology, and attaches great significance tothe ways in which inheritance interacts with the development ofphenotypes. This section contrasts this perspective on inheritancewith views that focus on replication. James Griesemer’sreproducer notion which combines inheritance and development ispresented. Finally, the relationship between inheritance systems andnotions of biological information is discussed.

2.1 Multi-generation reproduction of phenotypes

In contrast to the replicator view that looks for reliably replicatingentities that either produce copies of themselves, induce theproduction of such copies, or pass on their structure throughreplication processes (Dawkins 1976; Hull 1980), the views discussedin what follows see natural selection as depending on the reliablemulti-generation reproduction or reconstruction of phenotypes, andconceptualize inheritance accordingly (for related discussion of thetopics in this section and historical details see the entry onreplication). This perspective opens up many questions that the discussion ofinheritance systems attempts to address. First among these is howhereditary resources or inheritance processes affect the developmentof offspring so as to reliably reconstruct parental phenotypiccharacters; this question is shared more generally by developmentalevolutionary biology (Evo-Devo) and Developmental Systems Theory.Reconstruction typically occurs during the development of theoffspring, which is more or less independent from the parent, and maybe a complex, multi-stage, and temporally drawn out process. It mayinvolve more than one inheritance system and depend on interactionsbetween inheritance systems, depend on persistent environmentalresources such as sunlight and gravity as well as environmentalconditions produced by organisms and interactions with them (nicheconstruction), and depend on processes such as pattern formation thatgive rise to what might be characterized as emergent properties. Wenow turn to a discussion of inheritance thus construed vis-a-vis thenotion of replication.

2.2 Inheritance and replication

As mentioned earlier, two major influences led to the emphasis onreplication as a necessary condition for evolution via naturalselection: the influence of the replicator framework and the discoveryof the molecular basis of genetic inheritance, in particular DNAreplication. In their 1953 paper on the structure of DNA, James Watsonand Francis Crick famously noted that the properties of the doublehelix structure suggest a straightforward method for replicating theDNA sequence. It is now known that DNA replication issemiconservative: each of the strands of the double stranded DNAmolecule is used as a template for constructing a complementarystrand, and the replication process results in two DNA molecules, eachcontaining one of the original strands and one newly constructedstrand. In the absence of mutations, each of the new double strandedDNA molecules has the same sequence of base pairs (nucleotides) theoriginal DNA molecule had. DNA replication explains how theinformation in the DNA sequence is copied, so that when the celldivides each daughter cell ends up with a complete copy of theoriginal cell’s DNA. This is a critical element of geneticinheritance, though the genetic inheritance processes of mitosis andmeiosis are far more involved than DNA replication, which is only onecomponent of them.

When considered from the perspective of accounting for the reliablereconstruction of parental phenotypes, replication of the kind foundin genetic inheritance is seen to be neither sufficient nor necessaryfor heredity (Jablonka 2004, has a particularly clear discussion ofthese issues). The inheritance of cellular properties as a consequenceof self-sustaining metabolic loops, one kind of cellular epigeneticinheritance, is an example of inheritance not involving replicators.Partly on the basis of cellular epigenetic inheritance and similarobservations about other forms of extra-genetic inheritance, such asbehavioral and linguistic transmission, that do not conform with thereplicator framework, Jablonka has argued that thereplicator/interactor distinction should be rejected (Jablonka 2001,2004). More generally, she argued that “the replicator/vehicledichotomy… is meaningless in all cases in which thetransmission of information or the generation of new heritableinformation depends on development” (Jablonka 2001: 114).Godfrey-Smith (2009: sec. 2.4) discusses formal arguments showing thatreplicators are not a necessary condition for evolution by naturalselection.

DNA replication is also not sufficient for explaining cellularheredity, since cellular heredity depends on support from epigeneticnuclear and cytoplasmatic inheritance mechanisms that maintain propergene regulation. This point has been made during the historicaldebates about cytoplasmatic inheritance (Nanney 1958; Sapp 1987).Moreover, cellular epigenetic inheritance is essential for celldifferentiation in multi-cellular organisms, which involves theestablishment of lineages of cells that produce tissue specificphenotypes that are not due to differences in DNA sequence.Differentiated cells inherit their tissue-specificity, which theyusually do not alter throughout their life-cycle. This means that inaddition to its role in cellular heredity, cellular epigeneticinheritance is essential for the multi-generation reconstruction ofphenotypes of multi-cellular organisms, regardless of any direct roletransgenerational epigenetic inheritance plays in the transmission ofcharacters from parent to offspring above the cellular level, thoughsuch effects are also well known (see Jablonka & Raz 2009).

2.3 The reproducer concept

James Griesemer has proposed thereproducer as a fundamentalnotion for thinking about reproduction in evolution. A reproducer isan entity that multiplies with material overlap between parent andoffspring, transferring mechanisms conferring the capacity to developthe capacity to reproduce (Griesemer 2000a: S361, 2000b, 2000c, seealso the entry onreplication, section 8). By definition, being a reproducer is a propertyapplicable to systems that have developmental capacities. In contrastwith traditional accounts of natural selection that focus on heredity,Griesemer’s analysis of reproduction processes attempts tointegrate heredity and development in a single conceptual scheme.Godfrey-Smith has argued that both requirements emphasized byGriesemer — material overlap between generations, and thecapacity to develop — are too strong, and are not required for aformal account of evolution via natural selectionper se(Godfrey-Smith 2009: 83–84).

Based on the reproducer concept, Griesemer has proposed an analysis ofmodes of multiplication in which reproduction, inheritance, andreplication are special cases of multiplication processes (Griesemer2000a: S360; 2000c). According to this classification,inheritanceprocesses are reproduction processes in which there are evolvedmechanisms for producing hereditary relations in development.Replication processes in turn are inheritance processes withevolved coding mechanisms. Thus, replication (which is contrasted byGriesemer with mere copying) is a special case of inheritance, itselfa special case of biological reproduction. Genetic inheritance is areplication process and as such it involves coding mechanisms. Sincegenes do not constitute mechanisms of development in their own right,but are pieces of mechanisms, Griesemer argues that they cannot havethe privileged explanatory role often accorded to them (Griesemer2000a: 364). According to Griesemer’s classification, epigeneticinheritance processes can be classified as inheritance processes whichare not replication processes (Griesemer 2000c: 250).

Both Griesemer and Godfrey-Smith applied their respective notions ofreproducers to the question of collective reproduction, involvingentities that can reproduce but that contain other things than canalso reproduce (see Godfrey-Smith 2012, Griesemer 2018; for furtherdiscussion see entry onthe 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 ofcompositional organization, while Godfrey-Smith characterizescollective reproduction according to the degree of overall integrationof the reproducer, the degree of reproductive (germ/soma)specialization, and the degree of a reproductive bottleneck. Theproperties characterizing collective reproducers are arguably relatedto the inheritance systems involved (for one intriguing suggestionconcerned with the role of epigenetic inheritance in the origin of thegerm-line see Lachmann & Libby 2016).

Griesemer’s classification of reproducers is an abstractionhierarchy. It provides a formal taxonomy of reproducers, arrangingthem in a series of nested classes. The classification of inheritancesystems suggested by Jablonka and Lamb (Jablonka 2001; Jablonka &Lamb 2005/2014) discussed in the next section, in contrast, enumeratestypes 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 studyof inheritance systems in general, and extra-genetic inheritance inparticular, since on an abstract level inheritance may be thought ofas transmission of information or informational resources from parentto offspring (as opposed to the transmission of material resources).However, it is notoriously difficult to come up with notions ofinformation that are suitable for studying the various aspects ofbiological phenomena (see the entry onbiological 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 aunique developmental role is the claim that genes play aninformational role, not shared by other hereditary developmentalresources. The holistic view of inheritance articulated byDevelopmental Systems Theory downplays the significance of the ideathat inheritance should be conceived as the transmission ofinformation between generations (Griffiths & Gray 2001; Sterelny2001: 334, see also the discussion in Sterelny et al. 1996: 379). Inparticular, DST uses the so-calledparity argument to rejectthe view that DNA is uniquely informational while other inheritedresources merely provide material support for reading or interpretingDNA (Griffiths & Knight 1998). In recent work Griffiths applies aninformation-theoretic measure of causal specificity to measure how agiven factor contributes to the precise determination of thephenotype. This measure is produced by combining the classic notion ofmutual information, as found in Shannon information theory, withWoodward’s notion of speficity of causes (Woodward 2010).Griffiths (2017) argues that this framework naturally extends tovarious epigenetic marks and non-coding regions of DNA that arecausally specific, while at the same time distinguishing these casesfrom many other causes of the same outcomes, such as the presence ofRNA polymerase, that lack such specificity.

Jablonka (Jablonka 2001, 2002) introduced her discussion ofinheritance systems by characterizing them as systems that carryhereditary information, which in turn she defined as“thetransmissible organization of an actual or potential state of asystem” (cf. the different notion of information andrepresentation favored by Sterelny et. al. 1996). A common frameworkfor discussing hereditary information can then be used to compare andanalyze various inheritance systems and expose their differences aswell similarities (seesection 3.3).

3. Classification of Inheritance Systems

It is now fairly common in biological discourse to talk about variousforms of inheritance in addition to genetic inheritance. The two typesof inheritance most often referred to are probably cellular epigeneticinheritance and cultural and behavioral inheritance in humans andvarious animals. There is however no standardized or de facto systemor nomenclature used to classify inheritance systems and theirproperties. This is partly due to the wide range of hereditaryphenomena and the debates described earlier. A principled taxonomywould provide a guide for identifying inheritance systems, delimitingthem from one another, comparing their properties and possiblefunctions, and so on.

This section begins by making clear the distinction betweeninheritance systems and channels of inheritance. Various criteria thathave been proposed for identifying inheritance systems are thenpresented. The section concludes with a detailed discussion of theinfluential account of inheritance systems presented by Jablonka andLamb and a discussion of ecological inheritance and nicheconstruction.

3.1 Inheritance Channels

An important distinction betweeninheritance channels andinheritance systems should be made before classifyinginheritance systems. This distinction plays a central role incontroversies over classifying and delimiting inheritance systems.Simply put, inheritance channels refer to “routes acrossgenerations” (in the words of Sterelny et al. (Sterelny et al.1996: 390)) through which hereditary resources or information passfrom parent to offspring. The notion of inheritance system, incontrast, as used by Jablonka and Lamb in particular, is meant toclassify inheritance factors, mechanisms, and processes, and the waysin which they store and carry hereditary information (Jablonka 2001;Jablonka & Lamb 2005).

Multiple inheritance channels may be involved in the reconstruction ofthe phenotype. For example, as noted in the discussion of cellularheredity, inheritance of organelles during cell division is requiredfor the survival of daughter cells in addition to the inheritance ofthe nuclear genome. The role of multiple channels is particularlyapparent in cases where phenotypes depend on symbiotic associationsand thus on the transmission of symbionts. Examples of transmission ofsymbionts include: (1) The transmission of gut bacteria, which arerequired for digestion and for normal intestinal development, frommother to offspring. (2) Fungus-growing ants depend on the cultivationof fungus for food in underground gardens. When new queens leave theirparent colonies, they carry a fragment of the fungus with them to thesite of the new colony. (3) Various species of aphids, clams, andsponges allow some bacteria to pass through the oocytes from parent tooffspring, leading to vertical transmission parallel to genetictransmission. As a final example of multiple channels of inheritancenote that cultural transmission in humans and animals, which isrequired for the reconstruction of behavioral phenotypes such as birdsongs, food preferences, and other cultural traditions (Avital &Jablonka 2000), may also be considered to constitute supplementaryinheritance channels.

The same inheritance system may be used in multiple inheritancechannels. For example, the genetic inheritance system as defined byJablonka and Lamb is responsible for the inheritance of theinformation in the DNA in the eukaryotic nucleus and in the DNA ofmitochondria. Horizontal gene transfer more generally is considered byJablonka and Lamb to belong to the genetic system (Jablonka & Lamb2005:. 233), though it typically involves additional vectors ortransmission channels. Conversely, a single inheritance channel mayinvolve multiple inheritance systems, in the sense used by Jablonkaand Lamb. For example, DNA methylation, an epigenetic mark, copied incellular epigentic inheritance, is tied to the copying andtransmission of DNA. This arguably constitutes a single channel.Epigenetic mechanisms and heredity play a role in various propertiesof the genetic system, affecting things such as mutation andrecombination rates and hence genetic variation. Perhaps morefundamentally, epigenetic mechanisms are part of the mechanisms‘operating’ the genetic channel. The inheritance of thegenome, when a cell divides, involves recreation of the mothercell’s epigenetic state, a process that goes beyond copying(Lamm 2011, 2014; Lamm & Jablonka 2008).

While many interesting cases involve identifying new inheritancechannels which are based on new inheritance systems, and discussionsare often ambiguous as to which of the two notions they refer to, thestudy of inheritance systems is a separate endeavor from the analysisof the inheritance channels affecting individual organisms or traits.The holistic view about inheritance, found in Developmental SystemsTheory, rejects both the analysis of inheritance in terms of multiplesystems and in terms of multiple channels, arguing that bothdistinctions are at most convenient idealizations (Griffiths &Gray 2001), and it is not unusual for debates about holism to conflatethe discussion of the two issues. DST proponents argue that somedevelopmental resources are not easily represented as channels,especially persistent resources, that holism is more heuristicallyproductive, and that channels are not statistically independentinformation carriers (Griffiths & Gray 2001; see also the usefuldiscussion by Griesemer et al. (2005: 526)).

In response to the DST rejection of multiple channel accounts ofinheritance, Griesemer et al. (2005) note the multiple ways in whichchannels can be independent from one another. Channels may beindividuated as separate channels physically, chemically, orbiologically, regardless of whether they are statistically independentinformation channels. Additionally, causal independence should not berequired for individuating inheritance channels. While Jablonka andLamb use a notion of biological information to characterizeinheritance systems, they are not individuated based on statisticalindependence, but rather mechanistically (or, more accurately,mechanismically, that is by identifying classes of inheritancemechanisms) and by biological function.

3.2 Identifying and delimiting inheritance systems

As it is hereditary variations that are needed for evolution vianatural selection, Jablonka and Lamb set out to study differentinheritance systems (wheresystem is understood roughly tomean a set of interacting factors and mechanisms) by identifyingdifferent kinds of hereditary variation (Jablonka 2001; Jablonka &Lamb 1995, 2005/2014). Their approach can be described as focused onthe mechanismic basis for different types of hereditary phenotypicvariation. They have identified multiple inheritance systems, eachwith 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 asthe transmissible organization of an actual or potential state of asystem. A detailed account of their mechanismic classification ispresented insection 3.3.

A different approach to characterizing and possibly for identifyingand delimiting inheritance systems posits that to count as aninheritance system a system has to have evolved for the purpose oftransmitting hereditary information, i.e., to have the“meta-function” of producing heritable phenotypes (Shea2007). In this respect this approach is reminiscent of the extendedreplicator approach of Sterelny et al. (1996). Other requirements thathave been proposed in the literature are the demand for“unlimited” heredity, i.e., unlimited repertoire ofvariants the system can store and transmit, needed for sustained orcumulative evolution (see discussion in Godfrey-Smith 2000; MaynardSmith & Szathmáry 1995: 43), and the ability to generatefine-grained response to selection (see Griffiths 2001: 460). Boththese requirements regard genetic inheritance as having a privilegedrole in development and evolution in comparison with epigeneticinheritance processes. Jablonka and Lamb address these concerns withevolvability by noting that multiple instances of limited systems ofinheritance may exist within one cell (e.g., multiple self-sustainingmetabolic cycles), thus extending the repertoire of hereditaryvariations, and by emphasizing the effects limited hereditary systemscan have on the evolution of genetic variations (see the discussion ofgenetic assimilation below). Jablonka also argues that the requirementfor high fidelity of replication (e.g., Sterelny 2001) is not asnecessary for inheritance systems that employ filtering mechanismsthat ensure that transmitted variations are typically adaptive(Jablonka 2002). For further discussion of the requirement forevolvability see the discussion of Sterelny’s Hoyle conditionsinsection 4.6.

It should be noted that all the properties discussed above areproperties of systems, not properties of particular hereditaryrelations, of particular transmission events, or of replicatortokens.

3.3 Mechanismic Classification of Inheritance Systems

Jablonka and Lamb characterize four broadly defined inheritancesystems: two fairly specific inheritance systems — thegenetic inheritance system and thesymbolic inheritancesystem found in human languages — and two classes ofinheritance systems — cellular and organismalepigeneticinheritance systems andbehavioral inheritance systems.The systems are classified and grouped according to the way they storeand transmit variations and by the properties of the hereditaryrelations they give rise to.

Jablonka and Lamb’s classification of inheritance systems on thebasis of their mechanismic differences is not the only classificationapproach which focuses on hereditary variations. Recently,Helanterä & Uller (2010) analyzed the inheritance systemsJablonka and Lamb identified based on their evolutionary consequences.They claim that Jablonka and Lamb’s mechanismic classificationdoes not match a classification of means of inheritance according totheir evolutionary properties, and suggested classifying them intothree categories:vertical transmission which covers cases inwhich traits are transmitted from parent to offspring such as geneticinheritance and some epigenetic phenomena;induction whichcovers cases in which the environment determines change between parentand offspring such as induced genetic mutations and maternal effects;andacquisition which covers cases in which traits originatefrom non-parental individuals or other sources, for example horizontalgene transfer and various forms of learning. Similarly, Day andBonduriansky (2011), using a unified framework based on the PriceEquation, have argued that while the diversity of inheritancemechanisms is very large they give rise to a much more limited set ofinheritancepatterns, characterized as unique combinations ofreproductive transmission rules.

The properties of the inheritance systems that Jablonka and Lamb choseto study are those they deemed to be most pertinent for understandinginheritance, and its evolutionary consequences (Jablonka 2001: 100).In more recent work Jablonka and Lamb (2005/2014) distinguish betweenproperties of the way information is reproduced, and propertiesrelated to whether variation is targeted, responsive to theenvironment, or otherwise biased (the so-called “Lamarckiandimension”). Among the properties of reproduction of informationthat they identify are whether reproduction results from ordinarycellular activity and relies on general purpose cellular mechanisms orwhether 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 (referredto asvertical transmission) or to neighbors as well(horizontal transmission).

The properties related to targeting, constructing, and planning oftransmitted variation that Jablonka and Lamb identify are:

1. Is variation targeted, in the sense that the production ofvariants is biased towards producing some possible variants (i.e.,“non-random”)?
2. Is variation subject to developmental filtering and modificationbefore transmission, as found for example in behavioralinheritance?
3. Is variation constructed through direct planning by theorganisms?
4. Can variations change the selective environment, for example bychanging the environmental niche the organism occupies?

We now describe in more detail each of inheritance systems Jablonkaand Lamb identified. Jablonka’s and Lamb’s analysis ofinheritance systems is summarized in tables 1 and 2.

(The tables above are reproduced with permission from Eva Jablonka andMarion J. Lamb,Evolution In Four Dimensions: Genetic, Epigenetic,Behavioral, and Symbolic Variation In The History Of Life, MITPress 2005.)

3.3.1 The Genetic Inheritance System (GIS)

The genetic inheritance system (GIS) uses the nucleotide sequence innucleic acids, typically DNA, to store and transmit information (i.e.,hereditary variation), and includes the machinery responsible for DNAreplication, error correction etc. The GIS usesencodedinformation, as nucleotide sequences code for amino acids that formproteins using the genetic code which specifies which amino acidcorresponds to each triplet of nucleotides (called a codon). The DNAsequence also specifies functional RNA molecules. DNA nucleotides canbe modified independently of each other, a property referred to asmodular organization; it has been argued that codedinformation requires modular replication (Szathmáry 2000).Generally speaking, the genetic system providesunlimitedheredity, 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, areof course idealized assumptions. Unlimited heredity and modularity aremost often attributed to the genetic system as a whole, not only toprotein coding regions, and it is often argued that they are unique toit. Like the GIS, the symbolic inheritance system (discussed below),which is restricted to human beings, exhibits unlimited and modularheredity.

Various kinds of regulatory regions in DNA are spread throughout mostgenomes. They comprise “non-coding” sequences, in thesense that they do not code for proteins and do not depend on thegenetic code. Regulatory regions affect gene expression and chromatindynamics. It is still debated in the scientific community whetherthere are general properties of sequence organization that determinethese functions, which would suggest a high-order code. It should benoted that various non-coding sequences interact in specific ways withepigenetic mechanisms (such as DNA methylation and histonemodifications) in order to produce their regulatory effects. Thegenome which is the seat of genetic information is also a focal pointfor the operation of critical epigenetic mechanisms, and it may turnout not to be possible to fully understand the properties of thegenetic inheritance system and its evolution in isolation fromepigenetic inheritance (Jablonka & Lamb 2008; Lamm 2011,2014).

Some mechanisms that generate variation in DNA are invoked inparticular conditions (e.g., stress conditions), and produce variationthat 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 ofnon-directed processes that are not responsive to specific inducingconditions.

3.3.2 Epigenetic Inheritance Systems (EISs)

Epigenetic inheritance occurs when environmentally-induced anddevelopmentally-regulated variations, or variations that are theresult of developmental noise, are transmitted to subsequentgenerations of cells or organisms (Jablonka & Lamb 2005). The termepigenetic inheritance is used in a broad sense and in a narrow sense.The narrow sense refers to the systems that underlie cellularheredity. Four EISs in the narrow sense are discussed by Jablonka andLamb (2005/2014): (1) Self-sustaining steady-states of metaboliccycles. Transmission of the components of the cycle, such as proteinsand metabolites, can lead to reconstruction of the cycle in thedaughter cell. Self-sustaining loops can also maintain thetranscription levels of genes. For example, a transcriptionalself-sustaining loop is most likely responsible for white-opaqueswitching inCandida albicans, a change in phenotypic statethat involves a change in cell appearance, mating behavior, andpreferred host tissues that is heritable for many generations. (2)Structural inheritance of cell structures, such as cellular membranesand the cilia on the cell surface of ciliates. (3) Chromatin markingof various kinds that consists of molecular marks on chromosomes(specifically, DNA methylation and histone modifications, whichinvolve chemical groups attached to DNA and to proteins around whichthe DNA molecules are wrapped in eukaryotic cells). Some of thesemarks are copied by dedicated copying machinery, others seem to bereconstructed as a result of regular genome dynamics from partialmarkings transmitted to daughter cells (e.g., Henikoff, Furuyama,& Ahmad 2004; reviewed in Lamm 2014). (4) Inheritance of small RNAmolecules that affect gene expression. The most well-known caseinvolves RNA silencing (RNAi), a post-transcriptional silencingmechanism, though more and more classes of regulatory RNA moleculesand 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 andtransgenerational epigenetic inheritance through meiotic cells.Transgenerational heredity of DNA methylation has been observed inunicellular organisms, plants, and mammals, suggesting thattransgenerational epigenetic inheritance may be more prevalent thanoften suspected (Jablonka & Raz 2009). (2) Hereditary effects thatby-pass the germline, for example through early developmental inputsthat lead to regeneration of previous developmental conditions (e.g.,hormonal and neural conditions) and other forms ofphenotypictransmission, such as the transmission of symbionts andparasites, e.g., gut bacteria (Jablonka & Raz 2009).

In transgenerational epigenetic transmission, alternative phenotypescan persist for several, possibly many, generations, though theirpersistence may be more limited than that of genetic changes. They maythus have evolutionary effects in addition to the role played bycellular epigenetic inheritance in the development of multi-cellularorganisms that was noted above. Generally, epigenetic inheritancepiggybacks on general developmental and physiological mechanisms ofcells, and is a by product of other physiological functions, not theresult of an independent copying system that is content neutral; DNA methylation is anotable exception. Epigenetic inheritance typically isholistic rather than modular in its storage and transmission(i.e., it is not comprised of units of information that can be changedindependently of one another), and supports alimitedrepertoire of hereditary variants (e.g., the steady-states of ametabolic cycle). However, one cell may include many instances ofindependent self-sustaining metabolic cycles and structurallytransmitted cellular components, for example, increasing therepertoire of cellular variations that can be inherited via theseforms of inheritance. Typically, EISs (with some exceptions, such asDNA methylation) cannot transmit unexpressed (latent) information,although the transmission of partial factors or marks, which are notsufficient for expression, may be reliably sufficient when additionaldevelopmental factors are added.

3.3.3 Behavioral Inheritance Systems (BISs)

Jablonka and Lamb (Jablonka 2001; Jablonka & Lamb 2005) focus onthree types of behavioral inheritance: (1) Inheritance ofbehavior-affecting substances. The inducing substances bias thebehavior of offspring leading to limited behavioral heredity. Aparadigmatic case is the “transmission” of foodpreferences from mother to offspring via molecular cues passed throughthe placenta. (2) Non-imitative social learning that leads tosimilarity in behavior. Here, naive organisms learn throughinteraction with environmental circumstances that elicit particularbehavior and by observing the behavior of experienced adults, thoughnot by copying or imitating their behavior. A famous case ofnon-imitative social learning involved the spread of milk-bottleopening behavior in blue tits and great tits. It appears that thebehavior spread through the contact of birds with open milk-bottles orwith experienced birds using bottles as food sources, not by imitatingthe method of opening the bottles. (3) Imitation and instruction. Incontrast with the other behavioral inheritance systems, imitation ismodular (behavioral patterns are imitated independently of otherpatterns in the same behavioral sequence) and may depend on adedicated copying system or systems.

While the GIS and EISs transmit information mostly from parent tooffspring (i.e.,vertically), all behavioral inheritancesystems are directly or indirectly influenced by the socialenvironment, and are thus capable of transmitting information toneighbors as well, that ishorizontally. A second propertyshared by behavioral forms of inheritance is that for a behavior to betransmitted 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. Thesymbolic inheritance system shares some properties with the geneticinheritance system, notablymodularity,unlimitedvariability, the use ofcoded information, and thecapacity to transmitlatent information. Its origins are inbehavioral inheritance and it shares some of the properties ofbehavioral inheritance, in particular the capacity forhorizontaltransmission anddevelopmental filtering of variationprior to transmission.

Jablonka and Lamb’s account of cultural evolution in humansappeals to the properties of symbolic inheritance, most criticallythat variations are not blindly copied but rather reconstructed bylearners in ways that are sensitive to meaning, social context, andthe history of the individuals involved (Jablonka & Lamb2005/2014). They contrast their view with the meme based account ofcultural evolution presented by Dawkins and Blackmore (e.g., Blackmore1999), which takes cultural items to be stored in human brains andtransmitted to other human agents in the form of faithful replication,and cultural change to involve the differential success of replicationof the different cultural items. Jablonka and Lamb argue that focusingon replication and selection rather than on the generation of variantsand on reconstruction processes is particularly harmful forunderstanding cultural evolution.

3.4 Niche Construction Theory and Ecological Inheritance

Niche construction theory (Odling-Smee, Laland, & Feldman 2003)espouses the notion ofecological inheritance through whichprevious generations as well as current neighbors can affect organismsby altering the external environment or niche that they experience.This purportedly creates an inheritance channel that operates inparallel with genetic inheritance. Ecological inheritance is definedas the inheritance of selection pressures that were modified by nicheconstruction activities (Odling-Smee 2010: 176). Niche constructionleads to ecological inheritance if changes to the ecological nichepersist or accumulate and establish modified selection pressures. Notethat while the notion of ecological inheritance suggests viewing nicheconstruction as a transmission process, the focus on the modificationsdone to the niche highlights persistence. Extending the notion ofecological inheritance to the realm of development, Odling-Smee (2010:181) definesniche inheritance as the inheritance of aninitial organism-environment relationship, or “niche,”from ancestors. Niche inheritance can thus affect organisms’development directly, rather than through selection. For a recentdiscussion of the differences between selective niche construction anddevelopmental niche construction see Stotz (2017).

Odling-Smee et al. (2003) note that ecological inheritance “moreclosely resembles the inheritance of territory or property than itdoes the inheritance of genes.” In particular, it includestransmission of material resources that are difficult to construe asinformational. Odling-Smee (2010: 181) enumerates fundamentaldifferences between ecological inheritance and genetic inheritance:(1) Ecological inheritance is transmitted through an externalenvironment. It is not transmitted by reproduction. (2) Ecologicalinheritance need not depend on the transmission of discretereplicators (though this mechanism is not ruled out). (3) Ecologicalinheritance is continuously transmitted by multiple organisms, tomultiple other organisms, within and between generations, throughoutthe lifetime of organisms. (4) Ecological inheritance is not alwaystransmitted by genetic relatives. It should be noted that some ofthese properties of ecological inheritance are shared by extra-geneticinheritance more generally.

Odling-Smee (2010) distinguishes two transmission channels:transmission through direct connection during reproduction between theinternal environments of parent and offspring and transmission throughan external environment. In channel 1, the internal environment,Odling-Smee includes Jablonka’s and Lamb’s genetic andepigenetic inheritance systems, and some kinds of maternal effects. Inchannel 2, transmission through an external environment, he includesthe inheritance of modified selection pressures in the externalenvironments of organisms as a consequence of prior communicativeniche construction, and includes Jablonka’s and Lamb’sbehavioral and symbolic inheritance systems. All the inheritancesystems just mentioned transmit semantic information, according toOdling-Smee. In addition, both transmission channels are used totransmit energy and matter. Cytoplasmic inheritance of various kinds,and some kinds of maternal effects, are considered by Odling-Smee tobe energy and material resources transmitted through the internalenvironment, and traditional ecological inheritance of selectionpressures is non-semantic inheritance that is passed through anexternal environment.

4. Developmental and Evolutionary Implications

One of the best arguments for studying heredity through theperspective afforded by multiple inheritance systems is that thisperspective opens up questions about the evolutionary anddevelopmental relations and interactions between the variousinheritance systems that are characterized. Among these questions arequestions about whether each system creates new targets of selection,about the ways in which inheritance systems may provide developmentalscaffolding for other inheritance systems, about the regulatory rolethey may have in relation to one another, and about the evolution ofinheritance systems. We now turn to these issues.

Non-genetic inheritance can have an effect on the ecologicalconditions an organism faces by affecting or determining behavior andactivities, thus increasing or dampening selection. The result is afeedback loop between actions of the organism and selection that leadsto what Conrad Waddington referred to as the cybernetic nature ofevolution (Waddington 1961). Behavioral and symbolic inheritance, inparticular, can reinforce this process. By thus affecting theselective challenges faced by the organism, the evolutionary feedbackloop can turn short-term hereditary effects, that would not survivemany 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 biologicalevolution based on the multiple inheritance systems perspective. Theyargue that evolution can occur through any of the inheritance systemsthey identify (e.g., the behavioral) without necessarily involvinggenetic changes. This can happen through natural selection operatingon non-genetic hereditary variations. Epigenetic changes are usuallygenerated at a higher rate than genetic changes, often as a result ofchanges in environmental conditions, and the variation that isgenerated may have a higher chance of being beneficial than blindvariation. This may allow rapid adaptation to changing conditions.These claims apply to behavioral inheritance and symbolic inheritanceas well. Shea, Pen, & Uller (2011) distinguish between theadaptation resulting from selection on epigenetic variations, whichthey termselection-based effects, and the adaptationresulting from induced response to the environment, which they termdetection-based effects, and discuss their evolutionary anddevelopmental consequences. Selection-based effects lead to adaptationvia natural selection operating on reliably transmitted epigeneticvariations and are analogous to the selection-based effects of geneticinheritance, though epigenetic variation may occur more rapidly andits frequency may increase due to environmental challenges.Detection-based effects, in contrast, are the result of directionalvariation and are a form of phenotypic plasticity.

While Jablonka’s and Lamb’s approach is similar to that ofMaynard Smith & Szathmáry (Maynard Smith &Szathmáry 1995), in that Maynard Smith and Szathmáryfocus on changes in the way hereditary information is stored andtransmitted, Jablonka and Lamb argue that Maynard Smith andSzathmáry neglect the evolutionary role played by distinctinformation-transmitting systems. In particular, they argue thatMaynard Smith and Szathmáry’s approach neglects the roleof instructive processes, of the sort typically found in EISs, BISs,and the SIS, which lead to induced hereditary changes that are actedupon by natural selection (Jablonka & Lamb 2005: 343). MaynardSmith and Szathmáry, in contrast, argue that even with theexistence of epigenetic inheritance processes, natural selectionworking on mutations that are typically not adaptive (i.e.,non-directed) remains the fundamental evolutionary process (MaynardSmith & Szathmáry 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 beinvolved in the reproduction of organisms (let alone multiple kinds ofreplicators), questions about units of selection have to be addressed.As each inheritance system can lead to hereditary variations, theremay be multiple lineages related to the production of a singleorganism and even single phenotypic traits. Evolution may happen ineach lineage, and, in particular, each lineage may be“tracked” by natural selection.

According to the traditional view in evolutionary theory selectionoperates on individual organisms. This view can incorporate multipleinheritance systems and channels within a single evolutionary processby viewing each inheritance system or channel as providingdevelopmental resources for the construction of individual organisms,leading to a single evolutionary process operating on lineages oforganisms (qua interactors). Alternatively, lineages of phenotypictraits that may be affected by more than one inheritance system orchannel may be subject to selection. According to this view phenotypictraits 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 distinctevolutionary processes. The most prominent example of this line ofthought concerns the view that genes are supplemented by memes thatare units of cultural transmission, and each is manifested in aseparate evolutionary process: biological evolution operating onlineages of genes and cultural evolution operating on lineages ofmemes. The extended replicator framework, in contrast, accepts thepossibility of multiple kinds of replicators, but considers a singleevolutionary process that determines the fate of lineages of differentkinds of replicators by the success of their associated interactorsand extended phenotypic effects (Sterelny et al. 1996: 378).

4.2 Scaffolding

William Wimsatt and James Griesemer (2007) discuss multi-channelinheritance using the notion ofscaffolding fromdevelopmental psychology. Scaffolding refers to structures andfunctional processes that provide a supporting framework fordevelopment (see Caporael et al. 2013). Traits inherited through oneinheritance system can provide scaffolding for other inheritancesystems. Wimsatt and Griesemer suggest that if the flow of informationmust be scaffolded in such a way that carriers develop in appropriateconditions in order to assimilate, use, and carry the information,then the scaffolding must propagate or persist alongside theinformation in the channel — leading to multi-channelinheritance (Wimsatt & Griesemer 2007: 286). They suggest thatthis applies to any information that is sufficiently complex. As aconsequence it applies essentially to all biological and culturalphenomena.

A related notion is suggested by Peter Godfrey-Smith, who definesscaffolded reproducers as “entities which getreproduced as part of the reproduction of some larger unit (a simplereproducer), or that are reproduced by some other entity”(Godfrey-Smith 2009: 88). This notion is more restricted thanWimsatt’s and Griesemer’s appeal to scaffolding, as itonly refers to scaffolding of reproduction. Godfrey-Smith classifiesgenes as scaffolded reproducers since they rely on cellular machineryfor 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, theinheritance of the capacity for inheritance may itself involvedevelopmental reconstruction processes. These developmental processesmay depend on two types of resources: resources and cues from otherinheritance channels (e.g., the genetic system specifies elements ofthe brain, which are required for behavioral inheritance), and cuesthat are transmitted through the same channel and affect its furtherdevelopment (e.g., linguistic cues affecting linguistic abilities).Recent research on chromatin dynamics makes it clear that geneticinheritance relies on multiple epigenetic mechanisms, and suggeststhat we should be cautious with the distinction between a geneticinheritance system and cellular epigenetic inheritance systems (Lamm2011, 2014).

An interesting example from recent research is the suggestion thatsensorimotor experience plays a role in the development of thecapacity for imitation in the human brain (Catmur, Walsh, & Heyes2009). It is argued that if this model is correct, then “humanimitation is not only a channel, but also a product of culturalinheritance” (Catmur et al. 2009: 2376), since imitation notonly takes part in cultural inheritance, it is shaped by it as well.Thus, cultural inheritance may provide scaffolding for the developmentof imitation abilities in humans, which further affect behavioral andcultural inheritance.

4.4 Assimilation

One of the most interesting ways in which multiple inheritance systemscan interact evolutionarily is through processes such as theBaldwin Effect andgenetic assimilation. Thesenotions purport to explain how selection can drive developmentalresponses to environmental demands to become less dependent on thepresence of the external stimuli, and become increasingly hereditary(see Ancel 1999, 2000; Crispo 2007; Scheiner 2014, Weber & Depew2003). In these processes, non-genetic variants affect the selectionof genetic variations in favor of those that produce congruentphenotypic results (Jablonka & Lamb 2005/2014: chap. 7). In thesimplest case, originally discussed by Baldwin, a developmentalresponse to the environment allows organisms to survive and reproducefor enough generations for genetic mutations to accumulate throughnatural selection and make the developmental accommodation to theexternal stimulus unnecessary. The genetic mutations that are favoredare those that act in tandem with the developmental response. ConradWaddington characterized a process he termedgeneticassimilation leading to similar results, but emphasized the roleplayed by changes in combinations of genes and reorganization ofgenetic networks following the reshuffling of genes during the sexualprocess. The developmentally produced variants that lead theassimilation process need not be hereditary, and may be the result ofrecurrent plastic developmental responses in each generation. Whenthey are hereditary, however, their inheritance can reinforce theirspread in the population.

A similar phenomenon can result from processes of niche construction,which affect the selective environment faced by organisms and theirdescendants (Odling-Smee et al. 2003). A particularly well knownexample of the possible effects of cultural niche construction ongenetic evolution is the relationship between a history of dairyfarming in a culture and the prevalence of adults with a geneticvariant enabling them to continuously produce lactase, the enzymeneeded to digest fresh milk (Durham 1991; Mace 2009). This exampleillustrates how cultural evolution can drive genetic evolution, aelement of gene-culture coevolution.

Phenomena such as these may be characterized as being“Lamarckian” in flavor, even though they operate accordingto traditional Darwinian theory, since they provide room forinstructive or induced processes in evolution. The epigenetic,behavioral, and symbolic dimensions in evolution discussed by Jablonkaand Lamb produce induced variation which may affect evolution throughprocesses of assimilation as well as through their hereditary affects.In this way various inheritance systems other than the genetic canindirectly affect the evolution of genetic traits.

Assimilation may typically result in the response being partiallyrather than entirely independent of external stimuli. In other words,the response may become less dependent on external stimuli, and morebiased in favor of particular results, without becoming automatic.Jablonka and Lamb call this phenomenonpartial assimilation(Jablonka & Lamb 2005: 290), and see it as particularly importantfor understanding the way behavior (BISs) and language (the SIS)affect the evolution of mind. A further mechanism, identified byAvital and Jablonka, isassimilate and stretch. Here, given alimited and fixed capacity for learning, new learned elements may berecruited, when part of a behavioral sequence that formerly dependedon learning becomes genetically assimilated (Avital & Jablonka2000).

Alexander Badyaev suggests an evolutionary continuum of inheritancesystems that reflect the extent or stage of assimilation fromepigenetic (in the broad sense of Jablonka and Lamb) to geneticinheritance. Parental effects may be a transient stage along thiscontinuum, whose assimilation depends on the dynamics of theenvironment, and other constraints (Badyaev 2009; Badyaev & Uller2009; Helanterä & Uller 2010; see also: Yona et al.2015).

The overall picture that emerges from the consideration ofassimilation is of evolution driven by developmental capacities andbiases that affect which genetic mutations are selected. Mary-JaneWest-Eberhard summarized this observation with the claim that genesare typically followers in evolution rather than the ones leading theway (Jablonka 2006; West-Eberhard 2003).

4.5 Regulation and control

Already in 1958 David Nanney suggested that the difference betweengenetic and what we would now call cellular epigenetic inheritancelies not in their physical location (i.e., whether they lie in thenucleus or the cytoplasm), but rather that the genetic systemmaintains a set of “library specifications” while theepigenetic control system (to use his terminology) determineswhich specificities are expressed in each particular cell, accountingfor cell differentiation (Nanney 1958). Thus, according to Nanney, theepigenetic inheritance system plays a regulatory role in relation tothe genetic system.

Considering epigenetic control systems as providing a regulatoryfunction allowed Nanney to suggest that they may be expected to (1) beless stable, (2) be more susceptible to extrinsic control than geneticsystems, and (3) exhibit a limited number of “states”,since they are constrained by the information available in the geneticsystem at each particular time (Nanney 1958). These properties areindeed exhibited by the cellular epigenetic systems that have sincebeen identified, which play a role in cellular (e.g., genomic)regulation. DNA methylation and histone modifications can lead to genesilencing, for example. The transgenerational hereditary properties ofepigenetic markings may be subsequent to their regulatory function;however, in multicellular organisms, transgenerational heredity ofepigenetic marks is constrained by their developmental role, sinceparental epigenetic markings may have to be reset in gametes so thatthey can fulfill their developmental function anew in offspring (Sheaet al. 2011; see also Lachmann & Libby 2016).

4.6 Evolution of Inheritance Systems

Various suggestions have been made about the evolutionary historyunderlying the multiple systems of inheritance that have beenidentified and about their role in the evolution of life. In general,epigenetic inheritance allows rapid response to inducing stimuli andmay be more advantageous than mutation/selection cycles in specifictypes of fluctuating environments. This may be particularly importantin small populations and diploid organisms, in which mutations aretypically recessive (Nanney 1960). Maynard Smith and Szathmáryargued that evolution typically moves from limited to unlimitedsystems of inheritance or, to use their conceptual framework, fromlimited to unlimited hereditary replicators, and from holistic tomodular replication (Maynard Smith & Szathmáry 1995;Szathmáry 2000, 2015). This evolutionary trend is manifested inthe major transitions in evolution to new levels of individuality (andnew kinds of inheritance) that they have characterized. However, theco-existence of multiple systems of inheritance and its evolutionarysignificance is downplayed by such an account. Jablonka and Lamb(Jablonka 1994; Jablonka & Lamb 2006), in contrast, emphasize therole played by inheritance systems other than the genetic, inparticular by epigenetic inheritance, in evolutionary transitions.They place particular importance on the role of epigenetic inheritancein the evolution of multi-cellularity (see also Maynard Smith 1990;Nanney 1958, 1960; Shea et al. 2011) and in the evolution of thechromosome (Jablonka & Lamb 2006). Nanney (1960) suggested thatepigenetic inheritance played a role in cell specialization inunicellular populations (colonies), which conferred economic benefitsto individual cells and enabled populations to survive environmentaltraumas due to their heterogeneity, prior to the emergence of truemulti-cellularity. In addition, Jablonka (Jablonka 2001: 113) arguesthat with the evolution of repair and compensatory mechanismsinheritance systems become more limited. Two ways around theevolutionary stasis that would result are the move to higher levels ofindividuality (Jablonka 1994), and the transition to codedinformation. Ruth Sager (1966) suggested it may be adaptive to useinheritance systems minimizing variability to control traits that arecrucial for survival.

Kim Sterelny (2001) presented a set of requirements that aninheritance system (“replication system,” in his words)should meet if it is to support evolvability. Three fundamentalproperties are necessary: (1) blocking outlaws; (2) stabletransmission of phenotypes; (3) generation of variation. Using thesehigh-level desiderata, Sterelny articulates a series of nineconditions, called the Hoyle-conditions after Sterelny’s thoughtexperiment: a vertical, i.e., “only to offspring and fromparents” (C1), simultaneous (C2), and unbiased transmission (C3)of components (or replicators) that are irreversibly committed totheir biological role as replicators (C4). Further, to ensurestability, replication has to be high-fidelity (C5), and the mappingbetween replicators and system organization (i.e, “thegenotype-phenotype map”) has to be robust (C6). The requirementto support the generation of variation is cashed out in terms of beingable to support a large, if not unlimited, set of variants or, inSterelny’s framework, replicators (C7), having a“smooth” (quasi-continuous) mapping between replicatorsand system organization, i.e., small changes should result in smalleffects on organization (C8). Finally, the generation of biologicalorganization from replicators should be modular (C9), in the sensethat each replicator or small group of replicators should beresponsible for only one or a few traits. Whether an inheritancesystem fulfills the Hoyle conditions is a matter of degree. Clearly,the genetic system comes closest to meeting the full set of Hoyleconditions. Responding to Sterelny’s arguments, Griesemer et al.argue that we should direct our attention to the evolution ofinheritance systems (Griesemer et al. 2005). They note that the Hoyleconditions are a product of evolution, not a necessary preconditionfor inheritance that can support evolvability. In addition, they pointout that the Hoyle conditions may be met in adistributedmanner, that is by multiple inheritance systems each of which fails tomeet the criteria on its own but that together give rise to therequired properties. Griesemer et al. also argue that the Hoyleconditions may conflict: satisfying one may limit the ability tosatisfy others.

A significant aspect of the evolution of inheritance systems that isneglected by most contemporary accounts is the relationship betweenproperties of populations and fine-grained properties of inheritancesystems, in particular the relationship between the properties ofinheritance systems and the mating strategies of species. Thephenotypic variations produced by an inheritance system depend onpopulation level considerations such as these which determine, in thegenetic case, the frequency of heterozygotes (and hence thesignificance of dominance and recessivity) and the probability thatcalibrated gene networks will not be disrupted by sexual reproduction(e.g., because genes are adjacent on the chromosome or because thealleles are fixed in the relevant population). Population-levelconsiderations also apply to the analysis of epigenetic variation andinheritance. For example, population size may affect the evolutionaryconsequences of induced epigenetic variation (Rapp & Wendel 2005).Population level considerations are not typically addressed bycontemporary accounts of inheritance systems, yet clearly haveevolutionary implications.

This issue was central to Cyril Darlington’s analysis in his1939 bookThe Evolution of Genetic Systems (Darlington 1939).Darlington noted that the organization of the karyotype, or the“genetic system” to use his terminology, and its dynamicsthroughout the mating group, affect the hereditary combinations thatare produced, and hence hereditary variation, and can lead toreproductive isolation and speciation. The following quote gives thegeneral flavor of Darlington’s line of thought,

There must be a relationship between the hereditary materials, andtheir behaviour, throughout the whole group or species; and it is onthis relationship thegenetic system depends for itscharacter. Hybridity optimum, segregation, and recombination must allbe related throughout the group. Furthermore, they must be related notmerely amongst themselves, but also to the mating habits of theindividuals which compose the group, and to the barriers which makethat group by separating or isolating it from others. (Darlington andMather 1949: 237; their italics).

Darlington argued that the genetic system of a species is connected toits preference for inbreeding or outbreeding, since together theyaffect the frequency of heterozygosity (Darlington 1939; Darlington& Mather 1949). He noted that Mendelian inheritance establishes acycle between free and potential (latent) genetic variability(Darlington & Mather 1949: 276):Potential variability iscontained by heterozygotes, whilefree variability isexhibited by the phenotypes of their offspring as a result ofsegregation.

5. Conclusions

The study of inheritance systems attempts to synthesize recentdiscoveries about inheritance mechanisms and processes in nature withreflection about the nature and dynamics of evolutionary processes.The term “inheritance system” is typically used to referto both mechanisms and factors involved in inheritance, but the termlacks a standard definition which goes beyond enumerating variouspurported inheritance systems, and it is unclear if a singledefinition can capture the different uses of the term. A principleddefinition that determines how inheritance systems are individuatedand delimited—if indeed they can be— may be essential foraddressing many conceptual issues that remain open (see Griesemer etal. 2005). The lack of a universally accepted definition may explainthe fruitfulness of the term but also suggests approaching theliterature with caution.

The discussion above tried as much as possible to present a unifiedframework for the discussion of inheritance systems that is not tiedto any particular account. It contrasted the multiple inheritancesystems 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 onreproduction that underlies many discussions of inheritance systems(seesection 2).

The multiple inheritance system perspective highlights a variety ofquestions (seesection 4) and many fundamental questions remain open. Some of them depend onempirical work, perhaps most importantly determining the prevalenceand stability of transgenerational epigenetic inheritance(Helanterä & Uller 2010; Jablonka & Raz 2009; Shea et al.2011). The developmental aspects of many of the inheritance systemsdiscussed in this entry, in particular behavioral inheritance, arestill not fully understood. Generally, many open questions remainabout the interactions between the various systems and about theirevolution, in particular the evolution of social learning and theevolution of language. A crucial element downplayed by mostcontemporary accounts is the connection between population levelissues, such as population size, mating strategies, etc., and theproperties of inheritance systems. Addressing these issues requiresquantitative modeling, and eventually the integration of multipleinheritance systems with their different characteristics intopopulation genetics (see Day & Bonduriansky 2011, Geoghegan &Spencer 2012).

Several topics that are receiving significant attention in the biologyresearch community are directly related to the discussion ofinheritance systems. One is the invigorated field of culturalevolution and social learning (see Whiten 2017). A second area is thediscussion of inheritance of regulatory RNA molecules, an epigeneticinheritance process that goes beyond the transmission of RNA andinvolves developmental re-production (see Veigl 2017). A third area,already receiving significant attention from philosophers, is thehereditary properties and function of the microbiome. This is tied tothe recent interest in holobionts, a term that refers to assemblagesof multiple species, notably multi-cellular organisms and bacteria,that form ecological and potentially evolutionary units. It has beenargued by some researchers that holobionts are units of selection andthat the combined genome of the host and symbionts, dubbed ‘thehologenome’, is conceptually analogous to the genome, with thebacteria being analogous to genes. Arguably, this inheritance systemhas Lamarckian dimensions. Other researchers argue that the degree ofvertical transmission of symbionts is typically too low to qualify theholobionts as units of selection. For discussion of these issues seeHurst (2017), Opstal & Bordenstein (2015), and section IV ofGissis, Lamm & Shavit (2018). Finally, increasing knowledge of thegenetic system itself, in particular the role of chromatin shape anddynamics in gene expression as well as in mutation, recombination, andother fundamental processes, may lead to new perspectives on therelation between the genetic system and epigenetic mechanisms, andimprove our understanding of the transmission of chromatin state.Arguably, the DNA and non-DNA components of the genome should be seenand studied as a dynamic and responsive developmental system (Lamm2011, 2014). Moreover, better understanding of how genetic adaptationis reached under experimental conditions suggests how physiologicaland epigenetic responses may facilitate adaptation via other means,making a fitness improving response increasingly more robust, up topotentially becoming established via appropriate mutations (Yona etal. 2015). These results may lead to rethinking the dichotomy betweenplasticity and evolvability (Lamm & Jablonka 2008) and support theidea of “natural genetic engineering” systems (see Shapiro2011).

Non-genetic inheritance can have short term evolutionary effects andcan affect genetic evolution (e.g., through genetic assimilation).However, the long-term and macro-evolutionary significance ofnon-genetic inheritance, and in particular its effects on the waypopulations respond to selection is still being debated (e.g.,Helanterä & Uller 2010: 4). Jablonka’s and Lamb’sevolutionary views stress the role of “soft inheritance,”or the inheritance of acquired characters, which is exhibited by manyof the non-genetic inheritance systems. Partly on account of this theyare among those who raise the need to revise and extend the ModernEvolutionary Synthesis (Pigliucci & Müller 2010). The ModernSynthesis marginalized soft inheritance and viewed significantevolutionary change to be solely the result of gradual selectionworking on random variations. The assumptions underlying this view arechallenged by work on non-genetic inheritance.

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Other Internet Resources

• Tetrahymena Biogeography, David L. Nanney’s archive of historical and autobiographicaltexts about epigenetic inheritance in Tetrahymena.
• Cultural Evolution Society, lists resources and people in the multi-disciplinary field ofcultural evolution.
• Extended Evolutionary Synthesis: a website of a multinational, interdisciplinary consortium, puttingthe predictions of the Extended Evolutionary Synthesis (EES) to thetest. Includes many useful summaries and resources.

Related Entries

evolution: cultural |heritability |information: biological |replication and reproduction

Acknowledgments

The author thanks Adam Krashniak for help with the 2018 revision. The editors would like to thank Sally Ferguson for noticing andreporting a number of typographical and other infelicitous errors inthis entry.