The origins of microbial adaptations: how introgressive descent, egalitarian evolutionary transitions and expanded kin selection shape the network of life

MICROBIAL EVOLUTION: A GENEALOGICAL PERSPECTIVE Protists, bacteria and archaea (the prokaryotes), and their mobile genetic elements populate the microbial world. This world is ancient (several billion years old), numerically huge (with 5 × 1030 prokaryotic cells and 10–100 times more viruses!), and genetically extremely diversified. Such a large assemblage cannot be ignored in attempts to understand life’s history on Earth, however, how can biologists account for its evolution? For long, the notion of descent with modification, describing a process of vertical inheritance, defining a tree-like genealogical pattern, when the genetic material, modified by some mutations, is transferred from the genome of a last common ancestor to its direct progeny has offered a promising way to classify organisms and species. Thus, the origin of microbial adaptations can be searched for within lineages, in the changes of genetic material inherited from one ancestor. Yet, such studies are strongly constrained. Non-tree like evolution, generating a reticulate evolutionary pattern, cannot be analyzed with a genealogical tree. Moreover, viruses do not all originate from a single last ancestor (Lima-Mendez et al., 2008), nor do they all display obvious genealogical relationships with cellular organisms, hindering the collective study of mobile genetic elements and cells with a single tree. Genealogy also plays a central role for explaining the main types of behaviors described in the biological world: selfishness, mutualism, altruism, and spite (West et al., 2006). The evolution of these interactions can be understood by accounting for kinship between protagonists, under the standard assumption that genealogical proximity between individuals entails their genetic proximity (Huneman, 2013). Thus, knowing the relative kinship, the benefit for the recipient of an interaction and the cost for its actor allows determining when an individual cooperating with a kin, in ways enhancing its reproduction, or preventing distantly related members of a population to reproduce, actually maximizes the reproductive success and the survival of its own genes (van Baalen, 2013). Microbiologists are thus inclined to embrace the conceptual framework of kin selection to analyze many cooperations (Diggle et al., 2007). However, it is probably not enough to take genealogical relationships into account to explain the diversity, evolution, and interactions in the microbial world. Too systematic a focus on genealogy may even introduce some biases in the explanations of microbial diversity, evolution and interactions, because many crucial biological phenomena result from processes orthogonal to vertical descent.