Holobionts are multicellular eukaryotes with multiple species of persistent symbionts. They are not individuals in the genetic sense— composed of and regulated by the same genome—but they are anatomical, physiological, developmental, immunological, and evolutionary units, evolved from a shared relationship between different species. We argue that many of the interactions between human and microbiota symbionts and the reproductive process of a new holobiont are best understood as instances of reciprocal scaffolding of developmental processes and mutual construction of developmental, ecological, and evolutionary niches. Our examples show that mother, fetus, and different symbiotic microbial communities induce or constitute conditions for the development and reproduction of one another. These include the direct induction of maternal or fetus physiological changes, the restructuring of ecological relations between communities, and evolutionary selection against undesirable competitors. The mutual scaffolding and niche constructing processes start early—prior to amniotic rupture. We are evolutionarily, physiologically, and developmentally integrated holobiont systems, strung together through mutual reliance (developmental scaffolding) and mutual construction (niche construction). Bringing the processes of niche construction and developmental scaffolding together to interpret holobiont birth conceptually scaffolds two new directions for research: (1) in niche construction, identifying the evolutionary implications of organisms actively constructing multiple overlapping niches and scaffolds, and (2) in Evolutionary Developmental Biology, characterizing evolutionary and ecological processes as developmental causes.
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Genetic conflict may occur between genes expressed in parents and offspring, respectively (theory of parent-offspring conflict), or between genes in the offspring of material or paternal origin (parental conflict theory of genomic imprinting). The latter does not follow from the former.
This aspect of the holobiont solves the problem of cheaters in symbiosis (see Gilbert et al. 2012).
Whether or not C-sections predispose an infant to higher rates of infection is a debatable point because there does not seem to be good data. A widely cited study (MacDorman et al. 2006) claims that neonatal mortality is three-fold higher in those infants born by elective C-section (those C-sections not performed for medical reasons). However, given that C-sections are usually performed only when the physician perceives some risk, this is a difficult judgment to make (see Tuteur 2009). There is epidemiological evidence supporting a link between C-sections and asthma (Thavagnanam et al. 2008; Huang et al. 2014).
This quote from Lewontin accurately summarizes his position: “The metaphor of adaptation, while once an important heuristic for building evolutionary theory, is now an impediment to a real understanding of the evolutionary process and needs to be replaced by another. Although all metaphors are dangerous, the actual process of evolution seems best captured by the process of construction.” (Lewontin 2000: 40)
In these cases, it is misleading to speak of natural selection as a process of organisms adapting to the external environment when the organisms determine their environments. First, the environment changes when organisms change, either by phenotypic plasticity or by the genetic generation of new variations. Second, organisms actively modulate the environmental effects that are relevant to them. Therefore, the external environment alone cannot directly explain the outcomes of selection. Ecological developmental biology and the study of niche construction provide opportunities for an updated definition of microevolution that is grounded not on gene frequency changes but on the patterns of selection that result from environmental induction of phenotypes and the environmental manipulations of phenotypes (Walsh 2009; Blute 2008)
F. John Odling-Smee coined the term “niche construction” in his 1988 paper to present an alterative to Lewontin’s view as he “…overstated the case slightly. The idea that active organisms construct their own environments does not replace the idea of adaptation.” (Odling-Smee 1988: 75) The two views are briefly contrasted in this paper, but further development of their philosophical and conceptual differences, especially implications for the Modern Synthesis, will be elaborated in another paper.
The social environment is also an important target of niche construction (Saltz and Foley 2011).
Some philosophers argue that activities that do not alter the external environment are not instances of niche construction. For instance, some think that changes in experienced environment are just internal adaptations to an unchanging external environment (Godfrey-Smith 1998, 2001). Others argue that the notion of an experienced environment is just the idea that not all aspects of the external environment are relevant, and relevancy should be measured by taking into account features of the organism (Brandon 1990). A thorough discussion of this issue is beyond the scope of this paper. However, niche construction without changes in the environment makes a difference to development, ecology, and evolution when traits causally interact with the internal responses of organisms to the environment instead of the environment itself.
Given the genetically varied population of symbionts, birth scaffolds are chimeric as well as hybrid. Indeed, according to our new knowledge of holobionts, “chimeras” have been misclassified as being allies to faeries and unicorns. They now change taxonomic places with monogenetic organisms.
The process may not end with the two coming apart as autonomous individuals, but if so, each part—the scaffolding environment and the scaffolded system—is usually transformed. For example, the human mother and child are fundamentally changed after scaffolding each other (Caporael 2013) as a hybrid during the birth process.
In cognitive studies, difficulties are often framed in terms of complex computational problems for a system to solve. Scaffolds break down the complexity of a problem into manageable problems that are easier to compute. For instance, a classical paper on cognitive scaffolds distinguishes between actions that break down complex informational and problem spaces (epistemic actions) from actions that directly achieve a goal (pragmatic actions) (Kirsh and Maglio 1994).
Recent debates focus on how niche construction brings about reciprocal causation between developmental activities and evolutionary causes and the ramifications for the distinction or non-distinction of proximate and ultimate causes in biology (Laland et al. 2011).
See Aydede and Robbins (2009) for a general overview.
Previously, one of us suggested that niche construction may occur within a developing body, with gene products affecting the expression or selective environments on other genes of regulatory networks (Laland et al. 2008). These may form internal “environmentally mediated genotypic associations,” i.e. associations between genes within a single population or between multiple populations through niche construction. With reciprocal niche construction, there may be stronger and novel genotypic associations mediated by the constructed environments because the constructions are reciprocal.
Lewontin (2001) argues that an implication is that the selective coefficient is always frequency-dependent. Saltz and Nuzhdin (2014) are the first to model the evolutionary effects of local manipulation of varying developmental environments for a population of individuals with plastic traits in a single generation.
Aagaard, K., Riehle, K., Ma, J., Segata, N., Mistretta, T. A., Coarfa, C., et al. (2012). A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One, 7(6).
Aagaard, K., Ma, J., Antony, K. M., Ganu, R., Petrosino, J. & Versalovic, J. (2014). The placenta harbors a unique microbiome. Science Translational Medicine, 6(237).
Ardeshir, A., Narayan, N. R., Méndez-Lagares, G., Lu, D., Rauch, M., Huang, Y., et al. (2014). Breast-fed and bottle-fed infant rhesus macaques develop distinct gut microbiotas and immune systems. Science Translational Medicine, 6(252).
Aydede, M., & Robbins, P. (Eds.). (2009). The Cambridge handbook of situated cognition. Cambridge: Cambridge University Press.
Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., & Gordon, J. I. (2005). Host-bacterial mutualism in the human intestine. Science, 307(5717), 1915–1920.
Bickhard, M. H. (1992). Scaffolding and self scaffolding: Central aspects of development. In L. T. Winegar & J. Valsiner (Eds.), Children’s development within social contexts: Research and methodology (pp. 33–52). Hillsdale: Erlbaum.
Bickhard, M. H. (2005). Functional scaffolding and self-scaffolding. New Ideas in Psychology, 23(3), 166–173.
Blute, M. (2008). Is it time for an updated ‘Eco-Evo-Devo’ definition of evolution by natural selection? Spontaneous Generations: A Journal for the History and Philosophy of Science, 2(1), 1.
Brandon, R. N. (1990). Adaptation and environment. Princeton: Princeton University Press.
Brucker, R. M., & Bordenstein, S. R. (2013). The hologenomic basis of speciation: Gut bacteria cause hybrid lethality in the genus Nasonia. Science, 341(6146), 667–669.
Callebaut, W. (2007). Herbert Simon’s silent revolution. Biological Theory, 2(1), 76–86.
Caporael, L. R. (2013). Evolution, groups, and scaffolded minds. In L. R. Caporael, J. R. Griesemer & W. C. Wimsatt (Eds.), Developing scaffolds in evolution, culture, and cognition (pp. 57–76).
Caporael, L. R., Griesemer, J. R. & Wimsatt, W. C. (Eds.). (2013). Developing scaffolds in evolution, culture, and cognition. MIT Press:Cambridge.
Cash, H. L., Whitham, C. V., Behrendt, C. L., & Hooper, L. V. (2006). Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science, 313(5790), 1126–1130.
Chichlowski, M., De Lartigue, G., Bruce German, J., Raybould, H. E., & Mills, D. A. (2012). Bifidobacteria isolated from infants and cultured on human milk oligosaccharides affect intestinal epithelial function. Journal of Pediatric Gastroenterology and Nutrition, 55(3), 321–327.
Chu, H., & Mazmanian, S. K. (2013). Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nature Immunology, 14(7), 668–675.
Clark, A. (1989). Microcognition. Cambridge: MIT Press.
Clark, A. (2006). Language, embodiment, and the cognitive niche. Trends in Cognitive Sciences, 10(8), 370–374.
Conroy, M. E., Shi, H. N., & Walker, W. A. (2009). The long-term health effects of neonatal microbial flora. Current Opinion in Allergy and Clinical Immunology, 9(3), 197–201.
Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. M., & Relman, D. A. (2012). The application of ecological theory toward an understanding of the human microbiome. Science, 336(6086), 1255–1262.
Day, R. L., Laland, K. N., & Odling-Smee, F. J. (2003). Rethinking adaptation: the niche-construction perspective. Perspectives in Biology and Medicine, 46(1), 80–95.
Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., et al. (2010). Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proceedings of the National Academy of Sciences of the United States of America, 107(26), 11971–11975.
Donohue, K. (2005). Niche construction through phenological plasticity: life history dynamics and ecological consequences. New Phytologist, 166(1), 83–92.
Douglas, A. E. (2010). The symbiotic habit. Princeton: Princeton University Press.
Dunbar, H. E., Wilson, A. C. C., Ferguson, N. R., & Moran, N. A. (2007). Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biology, 5(5), 1006–1015.
Flynn, E. G., Laland, K. N., Kendal, R. L., & Kendal, J. R. (2013). Target article with commentaries: developmental niche construction. Developmental Science, 16(2), 296–313.
Franzenburg, S., Walter, J., Künzel, S., Wang, J., Baines, J. F., Bosch, T. C., & Fraune, S. (2013). Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proceedings of the National Academy of Sciences of the United States of America, 110(39), E3730–3738.
Fukuda, S., Toh, H., Hase, K., Oshima, K., Nakanishi, Y., Yoshimura, K., et al. (2011). Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature, 469(7331), 543–549.
Funkhouser, L. J. & Bordenstein, S. R. (2013). Mom knows best: the universality of maternal microbial transmission. PLoS Biol, 11(8): e1001631.
Garrido, D., Barile, D., & Mills, D. A. (2012). A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract. Advances in Nutrition, 3(3), 415S–421S.
Gilbert, S. F. (2014a). A holobiont birth narrative: The epigenetic transmission of the human microbiome. Frontiers in Genetics, 5.282. doi:10.3389/fgene.2014.00282.
Gilbert, S. F. (2014b). Symbiosis as the way of eukaryotic life: the dependent co-origination of the body. Journal of Biosciences, 39(2), 201–209.
Gilbert, S. F., & Epel, D. (2009). Ecological developmental biology. Sunderland: Sinauer Associates.
Gilbert, S. F., Sapp, J., & Tauber, A. I. (2012). A symbiotic view of life: we have never been individuals. Quarterly Review of Biology, 87(4), 325–341.
Godfrey-Smith, P. (1998). Complexity and the function of mind in nature. New York: Cambridge University Press.
Godfrey-Smith, P. (2001). Organism, environment, and dialectics. In R. S. Singh, C. B. Krimbas, D. B. Paul, & J. Beatty (Eds.), Thinking about evolution: Historical, philosophical, and political perspectives (pp. 253–266). New York: Cambridge University Press.
Good, M., Siggers, R. H., Sodhi, C. P., Afrazi, A., Alkhudari, F., Egan, C. E., et al. (2012). Amniotic fluid inhibits Toll-like receptor 4 signaling in the fetal and neonatal intestinal epithelium. Proceedings of the National Academy of Sciences of the United States of America, 109(28), 11330–11335.
Griesemer, J. R. (2014a). Reproduction and scaffolded developmental processes: An integrated evolutionary perspective. In A. Minelli & T. Pradeu (Eds.), Towards a theory of development (pp. 183–202). Oxford: Oxford University Press.
Griesemer, J. R. (2014b). Reproduction and the scaffolded development of hybrids. In L. R. Caporael, J. R. Griesemer & W. C. Wimsatt (Eds.), Developing scaffolds in evolution, culture, and cognition (pp. 23–55). MIT Press.
Haig, D. (1993). Genetic conflicts in human pregnancy. Quarterly Review of Biology, 68(4), 495–532.
Haig, D. (2000). The kinship theory of genomic imprinting. Annual Review of Ecology and Systematics, 31, 9–32.
Haig, D. (2004). Genomic imprinting and kinship: how good is the evidence? Annual Review of Genetics, 38, 553–585.
Haig, D. (2010). Transfers and transitions: parent-offspring conflict, genomic imprinting, and the evolution of human life history. Proceedings of the National Academy of Sciences of the United States of America, 107(SUPPL. 1), 1731–1735.
Haig, D. (2014). Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting. Heredity, 113(2), 96–103.
Hooper, L. V., Wong, M. H., Thelin, A., Hansson, L., Falk, P. G., & Gordon, J. I. (2001). Molecular analysis of commensal host-microbial relationships in the intestine. Science, 291(5505), 881–884.
Hooper, L. V., Stappenbeck, T. S., Hong, C. V., & Gordon, J. I. (2003). Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nature Immunology, 4(3), 269–273.
Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., et al. (2013). Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell, 155(7), 1451–1463.
Huang, L., Chen, Q., Zhao, Y., Wang, W., Fang, F. & Bao, Y. (2014). Is elective cesarean section associated with a higher risk of asthma? A meta-analysis. Journal of Asthma (0), 1–10.
Jakobsson, H. E., Abrahamsson, T. R., Jenmalm, M. C., Harris, K., Quince, C., Jernberg, C., et al. (2014). Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by Caesarean section. Gut, 63(4), 559–566.
Jiménez, E., Marín, M. L., Martín, R., Odriozola, J. M., Olivares, M., Xaus, J., et al. (2008). Is meconium from healthy newborns actually sterile? Research in Microbiology, 159(3), 187–193.
Jones, C. G., Lawton, J. H. & Shachak, M. (1996). Organisms as ecosystem engineers. In Ecosystem management (pp. 130–147). Springer-Verlag: New York.
Kendal, J., Tehrani, J. J., & Odling-Smee, F. J. (2011). Human niche construction in interdisciplinary focus. Philosophical Transactions of the Royal Society, B: Biological Sciences, 366(1566), 785–792. doi:10.1098/rstb.2010.0306.
Kirsh, D., & Maglio, P. (1994). On distinguishing epistemic from pragmatic action. Cognitive Science, 18(4), 513–549.
Koren, O., Goodrich, J. K., Cullender, T. C., Spor, A., Laitinen, K., Kling Bäckhed, H., et al. (2012). Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell, 150(3), 470–480.
Kylafis, G., & Loreau, M. (2008). Ecological and evolutionary consequences of niche construction for its agent. Ecology Letters, 11(10), 1072–1081.
Kylafis, G., & Loreau, M. (2011). Niche construction in the light of niche theory. Ecology Letters, 14(2), 82–90.
Laland, K. N., & O’Brien, M. J. (2010). Niche construction theory and archaeology. Journal of Archaeological Method and Theory, 17(4), 303–322.
Laland, K. N., & Sterelny, K. (2006). Perspective: seven reasons (not) to neglect niche construction. Evolution, 60(9), 1751–1762. doi:10.1111/j.0014-3820.2006.tb00520.x.
Laland, K. N., Odling-Smee, F. J., & Gilbert, S. F. (2008). EvoDevo and niche construction: building bridges. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 310B(7), 549–566. doi:10.1002/jez.b.21232.
Laland, K. N., Sterelny, K., Odling-Smee, F. J., Hoppitt, W., & Uller, T. (2011). Cause and effect in biology revisited: is Mayr’s proximate-ultimate dichotomy still useful? Science, 334(6062), 1512–1516. doi:10.1126/science.1210879.
Laland, K. N., Odling-Smee, F. J., & Turner, S. (2014). The role of internal and external constructive processes in evolution. Journal of Physiology, 592(11), 2413–2422.
Landmann, F., Foster, J. M., Michalski, M. L., Slatko, B. E., & Sullivan, W. (2014). Co-evolution between an endosymbiont and its nematode host: Wolbachia asymmetric posyterior localization and AP polarity establishment. PLoS Neglected Tropical Diseases, 8(8), e3096. doi:10.1371/journal.pntd.0003096.
Le Huërou-Luron, I., Blat, S., & Boudry, G. (2010). Breast- v. formula-feeding: impacts on the digestive tract and immediate and long-term health effects. Nutrition Research Reviews, 23(1), 23–36.
Lee, S. M., Donaldson, G. P., Mikulski, Z., Boyajian, S., Ley, K., & Mazmanian, S. K. (2013). Bacterial colonization factors control specificity and stability of the gut microbiota. Nature, 501(7467), 426–429.
Lehmann, L. (2007). The evolution of trans-generational altruism: Kin selection meets niche construction. Journal of Evolutionary Biology, 20(1), 181–189.
Levins, R., & Lewontin, R. C. (1985). The dialectical biologist. Cambridge: Harvard University Press.
Lewontin, R. C. (1978). Adaptation. Scientific American, 239, 157.
Lewontin, R. C. (1982). Organism and environment. In H. C. Plotkin (Ed.), Learning, development and culture (pp. 151–170). Chichester: Wiley.
Lewontin, R. C. (2000). The triple helix: Gene, organism and environment. Cambridge: Harvard University Press.
Lewontin, R. C. (2001 ). Gene, organism, and environment. In S. Oyama, P. E. Griffiths & R. D. Gray (Eds.), Cycles of contingency: Developmental systems and evolution. Cambridge: The MIT Press.
Lewontin, R. C. (2001). Gene, organism, and environment: A new introduction. In S. Oyama, P. E. Griffiths, & R. D. Gray (Eds.), Cycles of contingency: Developmental systems and evolution (pp. 55–57). Cambridge: The MIT Press.
Ley, R. E., Peterson, D. A., & Gordon, J. I. (2006). Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell, 124(4), 837–848.
Lievin, V., Peiffer, I., Hudault, S., Rochat, F., Brassart, D., Neeser, J. R., et al. (2000). Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut, 47(5), 646–652.
MacDorman, M. F., Declercq, E., Menacker, F., & Malloy, M. H. (2006). Infant and neonatal mortality for primary cesarean and vaginal births to women with “no indicated risk,” United States, 1998–2001 birth cohorts. Birth, 33(3), 175–182.
Makino, H., Kushiro, A., Ishikawa, E., Muylaert, D., Kubota, H., Sakai, T., et al. (2011). Transmission of intestinal Bifidobacterium longum subsp. longum strains from mother to infant, determined by multilocus sequencing typing and amplified fragment length polymorphism. Applied and Environmental Microbiology, 77(19), 6788–6793.
Makino, H., Kushiro, A., Ishikawa E., Kubota, H., Gawad, A., et al. (2013) Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant's microbiota. PLoS ONE 8(11), e78331
Martirosian, G., Kuipers, S., Verbrugh, H., Van Belkum, A., & Meisel-Mikolajczyk, F. (1995). PCR ribotyping and arbitrarily primed PCR for typing strains of Clostridium difficile from a Polish maternity hospital. Journal of Clinical Microbiology, 33(8), 2016–2021.
McCutcheon, J. P., & Von Dohlen, C. D. (2011). An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Current Biology, 21(16), 1366–1372.
McFall-Ngai, M., Hadfield, M. G., Bosch, T. C. G., Carey, H. V., Domazet-Lošo, T., Douglas, A. E., et al. (2013). Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110(9), 3229–3236.
Moran, N. A., Degnan, P. H., Santos, S. R., Dunbar, H. E., & Ochman, H. (2005). The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proceedings of the National Academy of Sciences of the United States of America, 102(47), 16919–16926.
Niess, J. H., Leithäuser, F., Adler, G., & Reimann, J. (2008). Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions. Journal of Immunology, 180(1), 559–568.
Ochman, H., Worobey, M., Kuo, C. H., Ndjango, J. B., Peeters, M., Hahn, B. H., & Hugenholtz, P. (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biology, 8(11), e1000546.
Odling-Smee, F. J. (1988). Niche-constructing phenotypes. In H. C. Plotkin (Ed.), The role of behavior in evolution (pp. 73–132). Cambridge: MIT Press.
Odling-Smee, F. J., Laland, K. N., & Feldman, M. W. (1996). Niche construction. The American Naturalist, 147(4), 641–648. doi:10.2307/2463239.
Odling-Smee, F. J., Laland, K. N., & Feldman, M. W. (2003). Niche construction: The neglected process in evolution. Princeton: Princeton University Press.
Odling-Smee, F. J., Erwin, D. H., Palkovacs, E. P., Feldman, M. W., & Laland, K. N. (2013). Niche construction theory: a practical guide for ecologists. The Quarterly Review of Biology, 88(1), 3–28. doi:10.1086/669266.
Oliver, K. M., Degnan, P. H., Hunter, M. S., & Moran, N. A. (2009). Bacteriophages encode factors required for protection in a symbiotic mutualism. Science, 325(5943), 992–994.
Otto, M. (2014). Physical stress and bacterial colonization. FEMS Microbiology Reviews, 38(6), 1250–1270.
Pradeu, T. (2011). A mixed self: the role of symbiosis in development. Biological Theory, 6(1), 80–88.
Prince, A. L., Antony, K. M., Chu, D. M. & Aagaard, K. M. (2014). The microbiome, parturition, and timing of birth: more questions than answers. Journal of Reproductive Immunology. 104–105:12–9. doi:10.1016/j.jri.2014.03.006.
Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464(7285), 59–65.
Rhee, K. J., Sethupathi, Driks, A., Lanning, D. K., & Knight, K. L. (2004). Role of commensal bacteria in development of gut-associated lymphoid tissues and preimmune antibody repertoire. Journal of Immunology, 172(2), 1118–1124.
Romero, R., Hassan, S. S., Gajer, Tarca, A. L., Fadrosh, D. W., Nikita, L., et al. (2014). The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome, 2(1), 4.
Round, J. L., O’Connell, R. M., & Mazmanian, S. K. (2010). Coordination of tolerogenic immune responses by the commensal microbiota. Journal of Autoimmunity, 34(3), J220–J225.
Sadedin, S. (2014). War in the womb: A ferocious biological struggle between mother and baby belies any sentimental ideas we might have about pregnancy. Aeon Magazine. http://aeon.co/magazine/science/pregnancy-is-a-battleground-between-mother-father-and-baby/ Accessed 20 Oct 2014
Saltz, J. B., & Foley, B. R. (2011). Natural genetic variation in social niche construction: social effects of aggression drive disruptive sexual selection in Drosophila melanogaster. The American Naturalist, 177(5), 645–654.
Saltz, J. B., & Nuzhdin, S. V. (2014). Genetic variation in niche construction: implications for development and evolutionary genetics. Trends in Ecology and Evolution, 29(1), 8–14.
Schell, M. A., Karmirantzou, M., Snel, B., Vilanova, D., Berger, B., Pessi, G., et al. (2002). The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proceedings of the National Academy of Sciences of the United States of America, 99(22), 14422–14427.
Scott‐Phillips, T. C., Laland, K. N., Shuker, D. M., Dickins, T. E., & West, S. A. (2014). The niche construction perspective: a critical appraisal. Evolution, 68(5), 1231–1243.
Sela, D. A., Chapman, J., Adeuya, A., Kim, J. H., Chen, F., Whitehead, T. R., et al. (2008). The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proceedings of the National Academy of Sciences of the United States of America, 105(48), 18964–18969.
Sela, D. A., Li, Y., Lerno, L., Wu, S., Marcobal, AM., German, JB., et al. (2011). An infantassociated bacterial commensal utilizes breast milk sialyloligosaccharides. J Biol Chem. 286: 11909–11918.
Sharon, G., Segal, D., Ringo, J. M., Hefetz, A., Zilber-Rosenberg, I., & Rosenberg, E. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 107(46), 20051–20056.
Simon, H. A. (1983). Reason in human affairs. Stanford: Stanford University Press.
Simon, H. A. (1996). The sciences of the artificial. Cambridge: MIT press.
Smith, M. I., Yatsunenko, T., Manary, M. J., Trehan, I., Mkakosya, R., Cheng, J., et al. (2013). Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science, 339(6119), 548–554.
Stappenbeck, T. S., Hooper, L. V., & Gordon, J. I. (2002). Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proceedings of the National Academy of Sciences of the United States of America, 99(24), 15451–15455.
Sterelny, K. (2003). Thought in a hostile world: The evolution of human cognition. Oxford: Wiley-Blackwell.
Sterelny, K. (2006). ‘Cognitive Load and Human Decision, or, Three Ways of Rolling the Rock Up Hill’, in Peter Carruthers, Stephen Laurence, Stephen Stich (ed.), The Innate Mind: 2: Culture and Cognition, Oxford University Press, United States, pp. 218–233.
Sterelny, K. (2010). Minds: extended or scaffolded? Phenomenology and the Cognitive Sciences, 9(4), 465–481.
Tannock, G. W., Fuller, R., & Pedersen, K. (1990). Lactobacillus succession in the piglet digestive tract demonstrated by plasmid profiling. Applied and Environmental Microbiology, 56(5), 1310–1316.
Tauber, A. I. (2008a). Expanding immunology: defensive versus ecological perspectives. Perspectives in Biology and Medicine, 51(2), 270–284.
Tauber, A. I. (2008b). The immune system and its ecology. Philosophy of Science, 75(2), 224–245.
Tauber, A. I. (2012). The biological notion of self and non-self. In E. N. Zalta (Ed.), The Stanford Encyclopedia of Philosophy (Summer 2012 Edition ed.) http://plato.stanford.edu/archives/sum2012/entries/biology-self/
Thavagnanam, S., Fleming, J., Bromley, A., Shields, M. D., & Cardwell, C. R. (2008). A meta-analysis of the association between Caesarean section and childhood asthma. Clinical and Experimental Allergy, 38(4), 629–633.
Tolman, E. C., & Brunswik, E. (1935). The organism and the causal texture of the environment. Psychological Review, 42(1), 43.
Trivers, R. L. (1974). Parent-offspring conflict. Integrative and Comparative Biology, 14(1), 249–264.
Turner, J. S. (2009). The extended organism: The physiology of animal-built structures. Harvard University Press,Cambridge.
Tuteur, A. (2009). Does C-section increase the rate of neonatal death? http://www.sciencebasedmedicine.org/does-c-section-increase-the-rate-of-neonatal-death/. Accessed 19 Oct 2014.
Underwood, M. A., Kalanetra, K. M., Bokulich, N. A., Lewis, Z. T., Mirmiran, M., Tancredi, D. J., et al. (2013). A comparison of two probiotic strains of bifidobacteria in premature infants. Journal of Pediatrics, 163(6), 1585–1591. e1589.
van Baalen, M., & Huneman, P. (2014). Organisms as ecosystems/ecosystems as organisms. Biological Theory, 9, 357–360.
Walsh, D. (2009). A commentary on Blute’s ‘updated definition’. Spontaneous Generations: A Journal for the History and Philosophy of Science, 2(1), 6.
Wikoff, W. R., Anfora, A. T., Liu, J., Schultz, P. G., Lesley, S. A., Peters, E. C., et al. (2009). Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proceedings of the National Academy of Sciences of the United States of America, 106(10), 3698–3703.
Wright, J. P., & Jones, C. G. (2006). The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. Bioscience, 56(3), 203–209.
Yoshida, E., Sakurama, H., Kiyohara, M., Nakajima, M., Kitaoka, M., Ashida, H., et al. (2012). Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology, 22(3), 361–368.
Zivkovic, A. M., German, J. B., Lebrilla, C. B., & Mills, D. A. (2011). Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proceedings of the National Academy of Sciences of the United States of America, 108(SUPPL. 1), 4653–4658.
This paper is dedicated to the late Werner Callebaut, who commented on the penultimate draft and pointed us to related sources prior to his unexpected passing. We miss him greatly. LC would also like to thank André Ariew and Weijen Liu for helpful discussions and Greg Dupuy for editorial suggestions.
Compliance with Ethical Standards
SFG is funded by the Academy of Finland and Swarthmore College. Our research does not involve any human or animal participants.
Conflict of interest
There are no potential conflicts of interest.
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Chiu, L., Gilbert, S.F. The Birth of the Holobiont: Multi-species Birthing Through Mutual Scaffolding and Niche Construction. Biosemiotics 8, 191–210 (2015). https://doi.org/10.1007/s12304-015-9232-5
- Niche construction
- Developmental scaffolding
- Evolutionary Developmental Biology