An emerging idea in evolutionary biology is that inheritance implies more than the sole transmission of the DNA sequence across generations. Non-genetic inheritance of information across generations results from various processes that contribute to parent–offspring resemblance, a property that is called heritability.
The concept of heritability has been generalized into that of inclusive heritability, which is the heredity of differences, including all forms of inheritance. It unifies genetic and non-genetic heritability into a single framework encompassing the multiple dimensions of inheritance. We briefly provide evidence for the four identified processes of non-genetic inheritance.
Epigenetic changes in DNA expression result in epigenetic inheritance when they are transmitted across generations, thus contributing to the transgenerational transmission of phenotypic variation. Epigenetic changes are usually mediated by changes in environmental conditions. Examples include the inheritance of maternal behaviour in rodents or the inheritance of flower symmetry.
Parental non-genetic effects can result in the inheritance of non-genetic information across generations, thus contributing to the non-genetic component of inclusive heritability. Examples include the inheritance of immunocompetence against given parasites in birds or flexible adaptation to the maternal light environment in plants.
Ecological inheritance occurs when offspring inherit the habitat of their parents. This indicates that any modification of the environment that results from ancestral activity and that affects fitness will change subsequent selective pressures. Examples include the webs, nests, dams and burrows that numerous animal species create, but also the changes in atmospheric gases and soil nutrients brought about by bacteria and plant species.
Culture is the part of phenotypic variance that is transmitted through social learning. Recent evidence suggests that cultural transmission is widespread among animals. Examples concern mate choice and species recognition. Cultural selection constitutes another engine of evolution when it interacts with natural selection in both animals and humans.
Non-genetic inheritance can easily be confounded with genetic inheritance. It is the intricate network of genetic and non-genetic inheritance systems that produce parent–offspring resemblance, which constitutes the whole evolutionary potential of a trait quantified by inclusive heritability.
We formally partition inclusive heritability and propose methods to disentangle its components in order to better integrate them into a comprehensive view of inheritance. We propose specific designs coupling field or experimental longitudinal data with animal model types of statistical tools.
Such methods should help to unravel fascinating enigmas in evolution and medicine, such as major evolutionary transitions or the 'missing heritability' in the human genome.
The time is ripe to broaden concepts of inheritance and heritability in order to fully grasp the richness of evolutionary processes, and we call for a multidimensional modern synthesis that would merge the current modern synthesis with an inclusive view of inheritance.
Many biologists are calling for an 'extended evolutionary synthesis' that would 'modernize the modern synthesis' of evolution. Biological information is typically considered as being transmitted across generations by the DNA sequence alone, but accumulating evidence indicates that both genetic and non-genetic inheritance, and the interactions between them, have important effects on evolutionary outcomes. We review the evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, and outline methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations. These issues have implications for diverse areas, from the question of missing heritability in human complex-trait genetics to the basis of major evolutionary transitions.
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We thank M. Hochberg, J. Odling-Smee, R. Bonduriansky, A. Whiten and L.-A. Giraldeau for their constructive comments on previous versions of this paper. R. H. Wagner, D. Réale, M. Morange, A. Barelli, J. Dodson, N. Destainville and D. Paèz also provided constructive suggestions. This work was supported by the French Agence Nationale de la Recherche (ANR-05-BLAN-0265, EVO-INF-ECOL to É.D. and ANR-08-JCJC-0041 to A.C.) and by a postdoctoral grant from the French Fondation Fyssen to S.B.
The authors declare no competing financial interests.
- Modern synthesis
The merging of Darwinism with genetics that occurred from the 1930s to the 1950s.
- Genome-wide association studies
(GWA studies). These are studies in which associations between genetic variation and a phenotype or trait of interest are identified by genotyping cases (for example, diseased individuals) and controls (for example, healthy individuals) for a set of genetic variants that capture variation across the entire genome. Tests of statistical association with a phenotype are performed locally along the genome.
The percentage of variation in a trait that is genetically transmitted to offspring.
- Inclusive heritability
The percentage of variation in a trait that is transmitted between generations, whatever the mechanism of transmission. Inclusive heritability should be greater than or equal to heritability.
Prion-forming proteins exist in different stable conformational states. In addition to a 'native' non-prion conformation, they occasionally fold into a prion conformation that replicates itself by templating the conformational conversion of other molecules of the same protein.
- Partible paternity
Situations in which children are believed to have more than one biological father and each of those men provides resources for the child, enhancing its chances of survival.
- Niche construction
This occurs when individuals modify their environments in such a way that it can affect their fitness, thus altering the selective pressures acting on them. Hence, members of many species inherit the cumulated environmental changes that previous generations have induced.
Evolutionary processes that occur above the species level and over protracted periods of geological time (for example, speciation, morphological change and extinction).
Sympatry is the condition in which the distributions of two species or differentiated populations overlap and hybridization between taxa would be possible if they were not reproductively isolated by factors other than spatial separation.
- Assortative mating
Nonrandom mating; it occurs when individuals select their mates on the basis of one or more physical or chemical characteristics. For instance, big males mate with big females and small males with small females.
- Social imprinting
The process by which young individuals of many vertebrates become imprinted on an object, usually their parents, observed during a critical period, usually very early in life. At the adult stage, social imprinting allows individual animals to recognize members of their own species with which to interact or mate. However, young individuals can be artificially imprinted on humans or any other object presented at the right time.
A social structure of species in which females spend their entire lives with close female relatives and form new groups primarily by group fissions.
The association between two variables that characterizes the tendency for the two variables to covary around their mean in a systematic way.
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Danchin, É., Charmantier, A., Champagne, F. et al. Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat Rev Genet 12, 475–486 (2011). https://doi.org/10.1038/nrg3028
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