Abstract
The current debate over extending inheritance and its evolutionary impact has focused on adding new categories of non-genetic factors to the classical transmission of DNA, and on trying to redefine inheritance. Transmitted factors have been mainly characterized by their directions of transmission (vertical, horizontal, or both) and the way they store variations. In this paper, we leave aside the issue of defining inheritance. We rather try to build an evolutionary conceptual framework that allows for tracing most, if not all forms of transmission and makes sense of their different tempos and modes. We discuss three key distinctions that should in particular be the targets of theoretical and empirical investigation, and try to assess the interplay among them and evolutionary dynamics. We distinguish two channels of transmission (channel 1 and channel 2), two measurements of the temporal dynamics of transmission, respectively across and within generations (durability and residency), and two types of transmitted factors according to their evolutionary relevance (selectively relevant and neutral stable factors). By implementing these three distinctions we can then map different forms of transmission over a continuous space describing the combination of their varying dynamical features. While our aim is not to provide yet another model of inheritance, putting together these distinctions and crossing them, we manage to offer an inclusive conceptual framework of transmission, grounded in empirical observation, and coherent with evolutionary theory. This interestingly opens possibilities for qualitative and quantitative analyses, and is a necessary step, we argue, in order to question the interplay between the dynamics of evolution and the dynamics of multiple forms of transmission.
Similar content being viewed by others
Notes
By factor we intend various sorts of physical entities and processes that are mechanistically transmitted and are involved in biological processes.
In this paper, we thus pay attention as much as possible not to use the term « inheritance » .
The more general issue of how to (re)define the notion of inheritance follows from these questions; however, as stated above, it will not be addressed in this paper.
In organisms with sexual reproduction, transmission via channel 1 involves the passage through a unicellular bottleneck associated with a specific type of cellular division: meiosis. Gametes are produced by meiosis and their fusion is the starting point of the development of the new organism. Transmission via bottleneck is a special, relatively frequent, case of transmission via channel 1: it is an evolved mechanism of transmission for a “fresh start” and is coupled with a developmental process. This specific feature of sexual reproduction perfectly fits the idea that factors transmitted through channel 1 travel from cell to cell directly, i.e., through a chain of cell divisions and fusions.
Even though material overlap does not prove to be a necessary feature for the transmission of something, it could be considered a guarantee of a more faithful transmission. This faithfulness is the consequence of the stability of the matter that is actually transmitted. We can think about the difference between written and oral transmission in an analogous way, with the example of a printed book and an oral (non-recorded) discourse: the former (imagine the book passed on to many people and read) is likely to be much more precise and faithful than the oral discourse after an equivalent number of people have repeated it.
As suggested by an anonymous referee, we see a major ontological difference between a hormone passed via cellular reproduction (in the egg yolk) and the same hormone being transmitted via the placenta: they differ in the transmission mechanisms involved. In the first case, this channel 1 type of transmission happens because of cell division (i.e., when the cytoplasmic content splits), and so only requires the availability and distribution of the hormone while the mechanism is taking place; whereas in the latter case, which we classify as a channel 2 transmission and in which the hormone is passed on through blood, the evolution of other complex structures with specific functions, such as the placenta, is required.
We specifically talk about the durability of a factor and not about the durability of its effect, the latter being more likely to have a shorter durability due to the inherent variability of the implementation of a factor into an effect (or, for genetics, the expression of a trait) and to the variability resulting from changes in the environment.
In principle, residency is also a measurement of the timing of transmission, i.e., it should allow for identifying when a factor is acquired during the life cycle of an individual organism and when it is lost; but these two points in time are in most cases very difficult to measure.
Selectively relevant factors are those that are actually considered to be heritable difference makers for which a measurement of heritability can be estimated, defined as a proportion of variance due to certain transmitted factors (i.e., genes according to the traditional gene-centered view of evolution; more factors, and not just genes, according to a broader, inclusive, conception of inheritance, e.g., Danchin et al. 2011). However, in this paper we do not think that transmitted factors are necessarily difference makers. Our present analysis covers all factors that are passed on from one organism to another by various transmission mechanisms, regardless of their selective value.
This means that the maintenance of some factor does not necessarily depend on the presence of standing variation in the population, so that factors that are important for the inheritance of some trait are functional and transmitted even though they are not variable. As suggested by an anonymous referee, this point relates to Mameli’s distinction between the inheritance of features (inheritanceF) and the inheritance of variation (inheritanceV); see Mameli 2005.
Shea et al. (2011) point to some related differences between epigenetic inheritance in plants and in animals. They express these in terms of their distinction between “selection-based” and “detection-based” epigenetic effects. Even though they can rely on the same epigenetic mechanisms (e.g., DNA methylation), these two types of effects have different functions: selection-based effects “carry adaptive information in virtue of selection over many generations of reliable transmission”, and detection-based effects “carry information about an environmental feature detected by the parent” (p. 8). Shea et al. suggest that, because of developmental reasons linked to the germ line-soma separation, detection-based effects may be less common in animals than in plants. Moreover, for selective reasons linked to the motility of animals and the fact that they have a nervous system, animals may have less need of epigenetic inheritance than plants. Finally, Shea et al. also suggest that, because of the extensive reprogramming of the epigenome in animals, long-term reliable transmission of epigenetic variants (i.e., high durability, in our terms), and so selection-based effects, will be rare. Thus, selection-based effects would, in our framework, be factors transmitted with high durability while detection-based effects display low durability. Still, both are evolutionary meaningful and the difference in transmission mechanisms in both cases results from selection.
References
Bonduriansky R, Day T (2009) Nongenetic inheritance and its evolutionary implications. Annu Rev Ecol Evol Syst 40:103–125
Bonduriansky R, Crean AJ, Day T (2012) The implications of nongenetic inheritance for evolution in changing environments. Evol Appl 5(2):192–201
Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29(3):386–397
Danchin E, Charmantier A, Champagne FA, Mesoudi A, Pujol B, Blanchet S (2011) Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat Rev Genet 12:475–486
Dawkins R (1976) The selfish gene. Oxford University Press, New York
Dawkins R (1982) The extended phenotype. The long reach of the gene. Oxford University Press, New York
Day T, Bonduriansky R (2011) A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am Nat 178:E18–E36
Dickins TE, Barton RA (2013) Reciprocal causation and the proximate-ultimate distinction. Biol Philos 28:747–756
Dickins TE, Dickins BJA (2008) Mother nature’s tolerant ways: why non-genetic inheritance has nothing to do with evolution. New Ideas Psychol 26:41–54
Dickins TE, Rahman Q (2012) The extended evolutionary synthesis and the role of soft inheritance in evolution. Proc R Soc B 279:2913–2921
Dimitriu T, Lotton C, Bénard-Capelle J, Misevic D, Brown SP, Lindner AB, Taddei F (2014) Genetic information transfer promotes cooperation in bacteria. Proc Natl Acad Sci 111(30):11103–11108
Furrow RE, Feldman MW (2014) Genetic variation and the evolution of epigenetic regulation. Evolution 68(3):673–683
Griesemer J (2000) Development, culture, and the units of inheritance. Philos Sci 67:S348–S2368
Heard E, Martienssen RA (2014) Transgeneration epigenetic inheritance: myths and mechanisms. Cell 157:95–109
Helanterä H, Uller T (2010) The price equation and extended inheritance. Philos Theory Biol 2:e101
Hull DL (1980) Indivuality and selection. Annu Rev Ecol Syst 11:311–332
Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, Cambridge
Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84(2):131–176
Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5(6):e1000530–e1000530
Kussell E, Leibler S (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309(5743):2075–2078
Laland KN, Uller T, Feldman MW, Sterelny K, Müller GB, Moczek A, Jablonka E, Odling-Smee J, Wray GA, Hoestra HE, Futuyama DJ, Lenski RE, Mackay TF, Schluter D, Strassmann JE (2014) Does evolutionary theory need a rethink? Nature 514:161–164
Laland KN, Uller T, Feldman MW, Sterelny K, Müller GB, Moczek A, Jablonka E, Odling-Smee J (2015) The extended evolutionary synthesis: its structure, assumptions and predictions. Proc R Soc B 282:20151019
Lewontin RC (1970) The units of selection. Annu Rev Ecol Syst 1:1–18
Mameli M (2004) Nongenetic selection and nongenetic inheritance. Br J Philos Sci 55:35–71
Mameli M (2005) The inheritance of features. Biol Philos 20:365–399
Mayr E (1982) The growth of biological thought: diversity, evolution, and inheritance. Belknap, Cambridge
Merlin F (forthcoming) Limited extended inheritance. In: Huneman P, Walsh D (eds) Challenges to evolutionary theory. Development, inheritance, adaptation. Oxford University Press, Oxford
Mesoudi A, Blanchet S, Charmantier A, Danchin E, Fogarty L, Jablonka E, Laland KN, Morgan TJH, Müller GB, Odling-Smee FJ, Pujol B (2013) Is non-genetic inheritance just a proximate mechanism? a corroboration of the extended evolutionry synthesis. Biol Theory 7(3):189–195
Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf EV, Muller MN, Pusey AE, Peeters M, Hahn BH, Ochman H (2016) Cospeciation of gut microbiota with hominids. Science 353(6297):380–382
Nogueira T, Rankin DJ, Touchon M, Taddei F, Brown SP, Rocha EP (2009) Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr Biol 19(20):1683–1691
Odling-Smee JF (2010) Niche inheritance. In: Pigliucci M, Müller GB (eds) Evolution: the extended synthesis. MIT Press, Cambridge, MA, pp 175–208
Odling-Smee JF, Laland KN, Feldman MW (2003) Niche construction. The neglected process in evolution. University Press, Princeton
Odumade OA, Knight JA, Schmeling DO, Masopust D, Balfour HH, Hogquist KA (2012) Primary Epstein-Barr virus infection does not erode preexisting CD8+ T cell memory in humans. J Exp Med 209(3):471–478
Pigliucci M, Müller GB (2010) Evolution: the extended synthesis. MIT Press, Cambridge
Pocheville A (2010) What Niche Construction is (not). In La Niche Ecologique: Concepts, Modèles, Applications. (Ph.D. Thesis). Ecole Normale Supérieure Paris, Paris. pp 39–124
Riboli-Sasco L, Taddei F, Brown SP (2013) Bacterial social life: information processing characteristics and cooperation coevolve. In: Joyce R, Calcott B, Sterleny K (eds) Cooperation and its evolution. MIT Press, Cambridge, pp 275–288
Richardson S, Daniels CR, Gillman MW, Golden J, Kukla R, Kuzawa C, Rich-Edwards J (2014) Society: don’t blame the mothers. Nature 512(7513):131–132
Rivoire O, Leibler S (2014) A model for the generation and transmission of variations in evolution. Proc Natl Acad Sci 111(19):E1940–E1949
Scott-Phillips TC, Dickins TE, West SA (2011) Evolutionary theory and the ultimate-proximate distinction in the human behavioral sciences. Perspect on Psychol Sci 6(1):38–47
Shea N, Pen I, Uller T (2011) Three epigenetic information channels and their different roles in evolution. J Evol Biol. doi:10.1111/j/1420-9101.2011.02235.x
Sperber D (2006) Why a deep understanding of cultural evolution is incompatible with shallow psychology. In: Enfield N, Levinson S (eds) Roots of human sociality. Culture, cognition, and interaction. Bloomsbury Academic, Oxford, pp 431–449
Sterelny K, Smith KC, Dickinson M (1996) The extended replicator. Biol Philos 11:377–403
Tanouchi Y, Pai A, Park H, Huang S, Stamatov R, Buchler NE, You L (2015) A noisy linear map underlies oscillations in cell size and gene expression in bacteria. Nature 523(7560):357–360
Uller T, Helanterä H (forthcoming) Heredity and evolutionary theory. In: Huneman P, Walsh D (eds) Challenges to evolutionary theory. Development, inheritance, adaptation. Oxford University Press, Oxford
van Opstal EJ, Bordenstein SR (2015) Rethinking heritability of the microbiome. Science 349:1172
Danchin E, Pocheville A, Rey O, Pujol B, Blanchet S (in prep) From nongenetic to genetic inheritance: epigenetics as a hub to genetic assimilation
Acknowledgments
We would like to thank the people of the Institut d’histoire et de philosophie des sciences et des techniques (Paris) belonging to the ANR project “ExplaBio”, in particular Philippe Huneman, as well as the anonymous referees for helpful objections and remarks.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Merlin, F., Riboli-Sasco, L. Mapping Biological Transmission: An Empirical, Dynamical, and Evolutionary Approach. Acta Biotheor 65, 97–115 (2017). https://doi.org/10.1007/s10441-017-9305-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10441-017-9305-8