Abstract
Research on symbiotic communities (microbiomes) of multicellular organisms seems to be changing our understanding of how species of plants and animals have evolved over millions of years. The quintessence of these discoveries is the emergence of the hologenome theory of evolution, founded on the concept that a holobiont (a host along with all of its associated symbiotic microorganisms) acts a single unit of selection in the process of evolution. Although the hologenome theory has become very popular among certain scientific circles, its principles are still being debated. In this paper, we argue, firstly, that only a very small number of symbiotic microorganisms are sufficiently integrated into multicellular organisms to act in concert with them as units of selection, thus rendering claims that holobionts are units of selection invalid. Secondly, even though holobionts are not units of selection, they can still constitute genuine units from an evolutionary perspective, provided we accept certain constraints: mainly, they should be considered units of co-operation. Thirdly, we propose a reconciliation of the role of symbiotic microorganisms with the theory of speciation through the use of a developed framework. Mainly, we will argue that, in order to understand the role of microorganisms in the speciation of multicellular organisms, it is not necessary to consider holobionts units of selection; it is sufficient to consider them units of co-operation.
Highlights
In the 1960s, the scientific community was astonished by demonstrations of previously hidden genetic diversity, both within and between individuals
The genome of the host and the genome of the microbiome constitute the genetic basis for its evolution. This is an important addition to the theory of evolution, bringing symbiotic microorganisms into the picture and initiating a debate about their significance and role in the evolution of multicellular organisms, thereby enabling a holistic view of the nature of species—one that is increasingly appreciated by both philosophers and biologists (Ley et al 2006; Gilbert et al 2012; Pradeu 2010, 2011; Hutter et al 2015), thanks to its basic emphasis on the fact that thinking of plants and animals, including humans, as autonomous biological individuals is a serious oversimplification
The question is: are holobionts at the very last stage of this process? In other words, are they so tightly integrated that they should be seen as representing a new level at which collective reproduction occurs? If we look at the relationships between hosts and symbiotic microorganisms, we realise that, there are many examples of interactions that have developed a level of interdependence leading to the emergence of collective reproducers
Summary
In the 1960s, the scientific community was astonished by demonstrations of previously hidden genetic diversity, both within and between individuals. A high level of integration might be achieved through aligning the process of reproduction, which ‘forces’ two units to co-operate because their fate is linked, or through evolving mechanisms to ‘find’ a partner in every succeeding generation because co-operation increases the fitness of both partners This is how holobionts undergo evolution, because they are basically a mix of vertically and horizontally inherited microbes. Its surface area is much smaller, and so it cannot interact with the entire holobiont, but only with certain host cells and with certain microbes in the vicinity This may seem to be a major disadvantage; if we recall that the idea of the hologenome was intended to basically capture the role of symbiotic microorganisms in the evolution of multicellular organisms (ZilberRosenberg and Rosenberg 2008), and that scientists still use it for that reason, the concept of a unit of co-operation seems to serve this purpose very well. It becomes clear that microbes may be responsible for the inviability of hybrids, because the functionality of the latter might be reduced due to the lack of specific microbes that, along with the host, make up a functional, cohesive whole
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