The Birth of the Holobiont: Multi-species Birthing Through Mutual Scaffolding and Niche Construction

Abstract

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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Notes

  1. 1.

    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.

  2. 2.

    This aspect of the holobiont solves the problem of cheaters in symbiosis (see Gilbert et al. 2012).

  3. 3.

    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).

  4. 4.

    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)

  5. 5.

    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)

  6. 6.

    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.

  7. 7.

    The social environment is also an important target of niche construction (Saltz and Foley 2011).

  8. 8.

    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.

  9. 9.

    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.

  10. 10.

    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.

  11. 11.

    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).

  12. 12.

    The relation between evolutionary modules, i.e. the requirement of near-decomposability (Simon 1996) and quasi-independence (Levins and Lewontin 1985) for evolvability, and developmental scaffolds as the decrease of modularity is an interesting topic to explore.

  13. 13.

    This idea harks back to Herbert Simon’s theory of bounded rationality (Simon 1983, 1996), that humans are cognitively limited and by nature reliant on organism-environment relations to make decisions. Simon is in turn inspired by Tolman and Brunswik’s (1935) classical paper.

  14. 14.

    See, for instance, discussions on cognitive offloading in humans, and humans as beings that engineer environments to support cognitive activities (Sterelny 2010, 2006, 2003).

  15. 15.

    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).

  16. 16.

    See Aydede and Robbins (2009) for a general overview.

  17. 17.

    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.

  18. 18.

    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.

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Acknowledgments

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.

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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

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Keywords

  • Holobionts
  • Birth
  • Niche construction
  • Developmental scaffolding
  • Evolutionary Developmental Biology