Evolutionary transitions revisited: Holobiont evo‐devo

Abstract

John T. Bonner lists four essential transformations in the evolution of life: the emergence of the eukaryotic cell, meiosis, multicellularity, and the nervous system. This paper analyses the mechanisms for those transitions in light of three of Dr. Bonner's earlier hypotheses: (a) that the organism is its life cycle, (b) that evolution consists of alterations of the life cycle, and (c) that development extends beyond the body and into interactions with other organisms. Using the notion of the holobiont life cycle, this paper attempts to show that these evolutionary transitions can be accomplished through various means of symbiosis. Perceiving the organism both as an interspecies consortium and as a life cycle supports a twofold redefinition of the organism as a holobiont constructed by integrating together the life cycles of several species. These findings highlight the importance of symbiosis and the holobiont development in analyses of evolution.

The holobiont concept before Margulis

“…Moreover, the very species studied by Meyer‐Abich are currently used again as model organisms to investigate the development and evolution of holobionts and other host‐microbiotes collectives: lichens (Aschenbrenner, Cernava, Berg, & Grube, 2016; Cernava et al, 2019), sponges (Pita, Fraune, & Hentschel, 2016; Webster & Thomas, 2016) and various plants, ranging from mosses, like Marchantia spp., to orchid species (Alcaraz et al, 2018; Hassani, Durán, & Hacquard, 2018; Jacquemyn, Waud, Merckx, Lievens, & Brys, 2015; Vandenkoornhuyse, Quaiser, Duhamel, Van, & Dufresne, 2015). Remarkably, current views of holobionts, both in evo‐devo and microbiology, share with Meyer‐Abich the assumption of the phylogenetic ubiquitous nature and evolutionary centrality of holobiosis (Gilbert, 2019; Gilbert et al, 2012; McFall‐Ngai et al, 2013; Rosenberg & Zilber‐Rosenberg, 2018). For him, nature was a “universal mycorrhiza” (Meyer‐Abich, 1943).…”

“…“Holobiont” is a concept that has been an attractor for several ideas, and researchers have independently converged on this word to describe the integrated composite organism composed of microbial and host eukaryotic species. In evolutionary developmental biology, particularly in eco‐devo and eco‐evo‐devo, recent conceptualizations of developmental and evolutionary systems as holobionts made possible new theoretical insights and showcased heuristic fruitfulness (see Bosch & Miller, 2016; Carrier & Reitzel, 2017; Collens, Kelley, & Katz, 2019; Gilbert, 2019; Gilbert, Bosch, & Ledón‐Rettig, 2015; Schwab, Casasa, & Moczek, 2019).…”

“Microbiota, symbiosis and individuality summer school” meeting report

“…The emerging consensus is that symbiotic microbes function in a similar way to host cells rather than as an aspect of the external environment, because they perform functions that were previously ascribed only to host cells. For example, microbiota allowed the evolution of herbivory through specialized digestion (Table 1 Gilbert's lecture; see also [4,22]) and microbiota facilitate functionality of the immune system (Table 1 Pradeu's lecture; see also [17]). Importantly, this happens regardless of the genetic difference between host cells and microbial cells.…”

“…What counts as an individual is question-dependent as different research contexts have different ways of characterizing individuality (Table 1 Pradeu's lecture; Gilbert's lecture; [4,17,36]). Some of the suggested conceptions of biological individuality have been evolutionary, ecological, immunological, and developmental [9,17,37,38].…”

“…This gathering was funded by the European Research Council through a Starting Grant to Thomas Pradeu for the project "Immunity, DEvelopment and the Microbiota-Understanding the Continuous Construction of Biological Identity" (IDEM). In light of the microbiota "revolution, " there is increasing recognition that the construction of biological identity includes a dynamic dialog with an organism's microbiota and is dependent on environmental factors [1][2][3][4][5]. A reexamination of biological identity and individuality is therefore needed.…”