Ecological inheritance

Ecological inheritance occurs when organisms inhabit a modified environment that a previous generation created; it was first described in Odling-Smee (1988) ^[1] and Odling-Smee et al. (1996) ^[2] as a consequence of niche construction. Standard evolutionary theory focuses on the influence that natural selection and genetic inheritance has on biological evolution, when individuals that survive and reproduce also transmit genes to their offspring. ^[3] If offspring do not live in a modified environment created by their parents, then niche construction activities of parents do not affect the selective pressures of their offspring (see orb-web spiders in Genetic inheritance vs. ecological inheritance below). ^[3] However, when niche construction affects multiple generations (i.e., parents and offspring), ecological inheritance acts a inheritance system different than genetic inheritance.

Since ecological inheritance is a result of ecosystem engineering ^{[4] [5]} and niche construction, the fitness of several species and their subsequent generations experience a selective pressure dependent on the modified environment they inherit. ^{[6] [3]} Organisms in subsequent generations will encounter ecological inheritance because they are affected by a new selective environment created by prior niche construction. ^[3] On a macroevolutionary scale, ecological inheritance has been defined as, "the persistence of environmental modifications by a species over multiple generations to influence the evolution of that or other species." ^[7] Ecological inheritance has also been defined as, "... the accumulation of environmental changes, such as altered soil, atmosphere or ocean states that previous generations have brought about through their niche-constructing activity, and that influence the development of descendant organisms." ^{[3] [7] [8]}

Related to niche construction and ecological inheritance are factors and features of an organism and environment, respectively, where the feature of an organism is synonymous with adaptation if natural selection favored it in response to an environmental factor. ^[9]  For example, a feature of the environment may have increased the fitness of an individual by enabling it to acquire a food resource or evade a predator more efficiently. In this context, natural selection promotes a correspondence between features and factors, defined as synerg. ^{[3] [9]} Ecological inheritance occurs when an organism experiences an altered factor-feature relationship with selected pressures originating from parents or ancestral generations. ^[3] Richard Lewontin stresses how by modifying the availability of biotic and abiotic resources, niche-constructing organisms can cause organisms to coevolve with their environments. ^[10]

Examples

In the book, On the Origin of Species, Charles Darwin described ways that organisms alter selection pressures by modifying local environments (i.e., habitats in which they live) that affect their fitness. ^[11] For example, the effect of ecological inheritance on long-term evolutionary dynamics are performed by subsequent generations of earthworm that burrow through soil. ^[6] As earthworms burrow, they modify soil structure and enrich the nutrient content by mixing decomposing organic matter with inorganic soil content. ^[6] The burrowing makes water easily available and absorbed by earthworms in the soil, and consequently, worms have kept their ancestral freshwater kidneys rather than evolve terrestrial anatomy. ^[6]

Ecological inheritance has significant implications for macroevolution. ^{[12] [13]} Ancestral species may modify environments through their niche construction that may have consequences for other species, sometimes millions of years later. ^{[13] [14]} For instance, cyanobacteria produced oxygen as a waste product of photosynthesis (see great oxygenation event), which dramatically changed the composition of the Earth’s atmosphere and oceans, with vast macroevolutionary consequences.

Ecological inheritance, ecosystem engineering, and niche construction

Almost all species engage in ecosystem engineering, which occurs when the availability of a resource is altered by organisms that create, alter, or destroy habitats. ^{[15] [16]} Niche construction occurs when the interactions and relationship between a species and its environment alters the niche and selective pressure of the species. ^[7] Organisms modify their local environment, or habitat, by relocating to a different location or physically altering the selective environment; when these modifications alter the selection of subsequent generations, ecological inheritance occurs. ^[7] Therefore, niche construction focuses on the evolutionary impact of species and their local environment. ^[7] Ecosystem engineering has been described as a consequence of niche construction ^[17] but it is not clear whether ecosystem engineering activities always influence selection. ^[7] Ecological inheritance has been termed a ‘persistor’ that may influence evolution when the persistence of ecological inheritance is longer than the timing of the ‘replicator’ – a term Richard Dawkins used for gene. ^{[18] [19]}

Genetic inheritance vs. ecological inheritance

Genetic inheritance depends on the processes of reproduction that transmit genes between generations, from parents to offspring. ^[6] Ecological inheritance takes the form of biotically modified selection pressure that can be passed on by organisms in one generation at any time in their lifetime to organisms of subsequent generations and can be thought of as subsequent generations of population inheriting a type of territory or property. ^[3] Ecological inheritance does not depend on replication of environmental factors, but rather on the persistence of environmental factors that affect the selective pressures of subsequent generations. ^[3] For example, the trait of web construction by orb-web spiders has been shaped by natural selection and is passed onto subsequent generations through genetic inheritance; spider webs are not a form of ecological inheritance because they are too transient and do not affect the evolution of multi-generational populations of spiders via niche construction. ^[3] If, however, the physical characteristics of a modified environment created by one generation continues to exist for the descendants, then niche construction is affecting more than one generation and ecological inheritance has occurred, as in the example of earthworms described above. ^[3]

In genetic inheritance, descendants inherit genes (acted upon by natural selection) from their parents that contain information in the nucleotide sequences of DNA used to express phenotypes; in ecological inheritance, information is not transmitted in the same way, but instead, characteristics of a modified environment affect the phenotypic expression of descendants. ^[20] The mechanisms of genetic and ecological inheritance are also different; whereas genetic inheritance depends on reproduction (e.g., sexual and asexual) where genes are transmitted in one direction from parent to offspring in the same species, the modified environment and its selective pressures caused by ecological inheritance can be handed down from one species to any other species within and between generations. ^[3]

The modern synthesis

Ecological inheritance is considered a form of habitat construction, which has been considered a new way to expand upon natural selection as a way organisms influence their own evolution. ^{[8] [21]} Two assumptions under the Modern Synthesis are the following: (1) only genes are inherited from one generation to the next and (2) micro-evolutionary processes that include selection, drift, mutation, and gene flow affect patterns of macro-evolution. ^[8] Since the early twentieth century, however, evolutionary biologists have modified the Modern Synthesis to include ways organisms modify the environment and inhabited by their subsequent generations. ^[8] This new interpretation of the Modern Synthesis is called the extended evolutionary synthesis and describes how ecological inheritance affects evolution on micro- and macro-evolutionary scales because organisms modify their environments in non-random ways to generate selective pressures on subsequent generations. ^[8]

References

1. Odling-Smee, F. J. (1988). Niche-constructing phenotypes. In H. C. Plotkin (Ed.), The role of behavior in evolution (pp. 73–132). The MIT Press.
2. Odling-Smee, F. John; Laland, Kevin N.; Feldman, Marcus W. (1996). "Niche Construction". The American Naturalist. 147 (4): 641–648. doi:10.1086/285870. ISSN   0003-0147. JSTOR   2463239. S2CID   222326061.
3. ODLING-SMEE, F. JOHN; LALAND, KEVIN N.; FELDMAN, MARCUS W. (2003). Niche Construction: The Neglected Process in Evolution (MPB-37). Princeton University Press. ISBN   978-0-691-04437-8. JSTOR   j.ctt24hqpd.
4. Jones, Clive G.; Lawton, John H.; Shachak, Moshe (October 1997). "Positive and Negative Effects of Organisms as Physical Ecosystem Engineers". Ecology. 78 (7): 1946–1957. doi:10.1890/0012-9658(1997)078[1946:PANEOO]2.0.CO;2. ISSN   0012-9658.
5. Jones, Clive G.; Lawton, John H.; Shachak, Moshe (1994), "Organisms as Ecosystem Engineers", Ecosystem Management, New York, NY: Springer New York, pp. 130–147, doi:10.1007/978-1-4612-4018-1_14, ISBN   978-0-387-94667-2 , retrieved 2023-05-10
6. Danchin, Étienne; Charmantier, Anne; Champagne, Frances A.; Mesoudi, Alex; Pujol, Benoit; Blanchet, Simon (July 2011). "Beyond DNA: integrating inclusive inheritance into an extended theory of evolution". Nature Reviews Genetics. 12 (7): 475–486. doi:10.1038/nrg3028. ISSN   1471-0056. PMID   21681209. S2CID   8837202.
7. Erwin, D (June 2008). "Macroevolution of ecosystem engineering, niche construction and diversity". Trends in Ecology & Evolution. 23 (6): 304–310. doi:10.1016/j.tree.2008.01.013. PMID   18457902.
8. Laland, Kevin N.; Uller, Tobias; Feldman, Marcus W.; Sterelny, Kim; Müller, Gerd B.; Moczek, Armin; Jablonka, Eva; Odling-Smee, John (2015-08-22). "The extended evolutionary synthesis: its structure, assumptions and predictions". Proceedings of the Royal Society B: Biological Sciences. 282 (1813): 20151019. doi:10.1098/rspb.2015.1019. ISSN   0962-8452. PMC   4632619 . PMID   26246559.
9. Bock, Walter J. (1980). "The Definition and Recognition of Biological Adaptation". American Zoologist. 20 (1): 217–227. doi:10.1093/icb/20.1.217. ISSN   0003-1569. JSTOR   3882363.
10. Lewontin, Richard C. (1983). "Gene, Organism and Environment". In Bendall, D. S. (ed.). Evolution from Molecules to Men . Cambridge University Press. ISBN   9780521289337.
11. Darwin, Charles (2008-11-13), "hybridism", On the Origin of Species, Oxford University Press, doi:10.1093/owc/9780199219223.003.0010, ISBN   978-0-19-921922-3 , retrieved 2023-05-10
12. Odling-Smee, F. John (2003). Niche Construction. Princeton, New Jersey: Princeton University Press. ISBN   978-0-691-04437-8.
13. Erwin, Douglas H. (2008). "Macroevolution of ecosystem engineering, niche construction and diversity". Trends Ecol Evol. 23 (6): 304–310. doi:10.1016/j.tree.2008.01.013. PMID   18457902.
14. Erwin, Douglas H.; Valentine, James W. (2013). The Cambrian Explosion: The Reconstruction of Animal Biodiversity. Greenwood Village, Colorado: Roberts and Company. ISBN   978-1-936221-03-5.
15. Jones, Clive G.; Lawton, John H.; Shachak, Moshe (1997). "Positive and Negative Effects of Organisms as Physical Ecosystem Engineers". Ecology. 78 (7): 1946–1957. doi:10.2307/2265935. ISSN   0012-9658. JSTOR   2265935.
16. Jones, Clive G.; Lawton, John H.; Shachak, Moshe (1994), "Organisms as Ecosystem Engineers", Ecosystem Management, New York, NY: Springer New York, pp. 130–147, doi:10.1007/978-1-4612-4018-1_14, ISBN   978-0-387-94667-2 , retrieved 2023-03-28
17. Odling-Smee, F. John (2003). Niche construction : the neglected process in evolution. Kevin N. Laland, Marcus W. Feldman. Princeton: Princeton University Press. ISBN   978-1-4008-4726-6. OCLC   827947192.
18. Turner, J. Scott (2004-06-01). "Extended Phenotypes and Extended Organisms". Biology and Philosophy. 19 (3): 327–352. doi:10.1023/B:BIPH.0000036115.65522.a1. ISSN   1572-8404. S2CID   10994912.
19. Dawkins, Richard (2004-06-01). "Extended Phenotype – But Not Too Extended. A Reply to Laland, Turner and Jablonka". Biology and Philosophy. 19 (3): 377–396. doi:10.1023/B:BIPH.0000036180.14904.96. ISSN   1572-8404. S2CID   85750258.
20. Jones, Clive G.; Lawton, John H., eds. (1995). Linking Species & Ecosystems. doi:10.1007/978-1-4615-1773-3. ISBN   978-1-4613-5714-8. S2CID   9103443.
21. Lewontin, Richard C. (1974). The Genetic Basis of Evolutionary Change. Columbia University Press. ISBN   0-231-03392-3.

Further reading

• Odling-Smee, F. John (2010). "Niche Inheritance". In Pigliucci, Massimo; Müller, Gerd B (eds.). Evolution: The Extended Synthesis. MIT Press. doi:10.7551/mitpress/9780262513678.001.0001. ISBN   978-0262513678. Frames ecological inheritance in the broader context of niche inheritance.
• Odling-Smee, F. John; Laland, Kevin N. (2011). "Ecological inheritance and cultural inheritance: what are they and how do they differ?". Biological Theory. 6 (3): 220–230. doi:10.1007/s13752-012-0030-x. S2CID   85409192. Compares ecological and cultural inheritance.