Microorganisms as scaffolds of host individuality: an eco-immunity account of the holobiont

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 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 without their scaffolding microorganisms.

Can't see the colony for the bees: behavioural perspectives of biological individuality

“…Because Wolbachia are able to spread horizontally from host to host (Heath et al ., ; Raychoudhury et al ., ), they are not considered to be part of the evolutionary individual. Similarly, we do not support the idea that the ‘hologenome’ should be considered as part of the evolutionary individual (as Zilber‐Rosenberg & Rosenberg, do, but see also Chiu & Eberl, ; Moran & Sloan, ; Queller & Strassmann, ; Skillings, ) – but this debate is beyond the scope of this review.…”

The many faces of biological individuality

“…Finally, several contributors pay attention to what the field of ecology has to say about biological individuality, including David Queller and Joan Strassmann (2016), Derek Skillings (2016), and, in an ''ecological-developmental'' perspective, Gilbert and Tauber (2016) as well as Chiu and Eberl (2016).…”

“…Pradeu (2016) defends the view that, from an immunological point of view, a biological individual is made of all the components that are immunologically tolerated, which include many (but not all) microbes found in or on a host. Chiu and Eberl (2016) assert that microorganisms are constitutive of host immunity as external scaffolds, varying in degrees of reliability, specificity, and exclusivity. In their view, even if holobionts are not internally integrated enough to qualify as organisms or units of selection, they are still individuals in a different and more general way: the holobiont must be seen as the host plus the microorganisms that scaffold its immunity.…”

What Is a Hologenomic Adaptation? Emergent Individuality and Inter-Identity in Multispecies Systems

“…The idea, notwithstanding, has been faced with some criticism on the basis that firstly, the hypothesis that the holobiont is a biological individual is not precise enough to be biologically significant (Godfrey-Smith, 2013;Booth, 2014;Chiu and Eberl, 2016;Queller and Strassmann, 2016;Skillings, 2016). Secondly, the claims, assumptions, and implications concerning the biological individuality of holobionts does not seem to be completely supported by our current empirical evidence (Moran and Sloan, 2015;Douglas and Werren, 2016;Hurst, 2017;Bourrat and Griffiths, 2018;Stencel and Wloch-Salamon, 2018).…”

“…Thus, in that view, most authors had argued that the identity of the holobiont is not temporally preserved, as the microbiome species composition can sometimes be very unstable during the lifetime of the host. 16 Chiu and Eberl (2016) have recently presented the most elaborated version of this argument. They join three pieces of evidence to support their view.…”