ACADEMIC Publications

Abstract: Gut microbiota have played important roles in the evolutionary transition from carnivory to herbivory. In the evolution of ruminants, three modes of macrobe-microbe symbiosis have facilitated the phenotypic switch into a new nutritional mode. Mutualistic microbes acquired during birth enable the building of the rumen (developmental symbiosis), the digestion of plant fiber (nutritional symbiosis), and the detoxification of plant toxins (protective symbiosis). These symbioses created a new plant dietary niche through two types of niche construction: “perturbational niche construction,” a phenotypic process whereby gut microbes initiate the building of a mature rumen from the nonfunctional anlagen of this stomach region; and “mediational niche construction,” whereby microbe-induced changes alter how the animal experiences environmental resources without actual modification of the environment. Thanks to microbes, plants are now edible. We argue that the reciprocal niche construction of the host and its associated microbial organisms (i.e., the “holobiont”) scaffold each other’s developmental and phenotypic processes as well as organize a new selective environment of the holobiont as a whole.

Evolutionary theory is dominated by externalist models, theories, strategies, and metaphors that appeal to the environment to explain adaptive fit, or "good design." Niche construction challenges these externalist explanatory strategies, however, current versions of niche construction theory focus only on the evolutionary and causal significance of constructed environments that are intrinsically defined by environmental properties, not defined in relation to the organisms. In this chapter, I make the case for the evolutionary significance of "experiential niche construction" (coined by Sultan 2015).

Abstract: Resident microbiota do not just shape host immunity, they can also contribute to host protection against pathogens and infectious diseases. Previous reviews of the protective roles of the microbiota have focused exclusively on colonization resistance localized within a microenvironment. This review shows that the protection against pathogens also involves the mitigation of pathogenic impact without eliminating the pathogens (i.e., “disease tolerance”) and the containment of microorganisms to prevent pathogenic spread. Protective microorganisms can have an impact beyond their niche, interfering with the entry, establishment, growth, and spread of pathogenic microorganisms. More fundamentally, we propose a series of conceptual clarifications in support of the idea of a “co-immunity”, where an organism is protected by both its own immune system and components of its microbiota.

Abstract: Though the immune system is generally defined as a system of defense, it is increasingly recognized that the immune system also plays a crucial role in tissue repair and its potential dysregulations. In this review, we explore how distinct immune cell types are involved in tissue repair, and how they interact in a process that is tightly regulated both spatially and temporally. We insist on the concept of immune cell plasticity which, in recent years, has proved fundamental for the success/understanding of the repair process. Overall, the perspective presented here suggests that the immune system plays a central role in the physiological robustness of the organism, and that cell plasticity contributes to the realization of this robustness.

Abstract: There is currently a great debate about whether the holobiont, i.e. a multicellular host and its residential microorganisms, constitutes a biological individual. We propose that resident microorganisms have a general and important role in the individuality of the host organism, not the holobiont. Drawing upon the Equilibrium Model of Immunity (Eberl in Nat Rev Immunol 16:524–532, 2016), we argue that microorganisms are scaffolds of immune capacities and processes that determine the constituency and persistence of the host organism. A scaffolding perspective accommodates the contingency and heterogeneity of resident microorganisms while accounting for their necessity and unifying contributions to host individuality. In our symbiotic view of life, holobionts may not be organisms or units of selection, but macroorganisms cannot persist nor function as individuals without their scaffolding microorganisms.

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.