Charles J. Goodnight

Experimental studies of group selection show that higher levels of selection act on indirect genetic effects, making the response to group and community selection qualitatively different from that of individual selection. This suggests that multilevel selection plays a key role in the evolution of supersocial societies. Experiments showing the effectiveness of community selection indicate that we should consider the possibility that selection among communities may be important in the evolution of supersocial species.

Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organization—what is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon.

Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organization - What is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon. For instance, critiquing the hologenome concept is not synonymous with critiquing coevolution, and arguing that an entity is not a primary unit of selection dismisses that the hologenome concept has always embraced multi-level selection. Holobionts and hologenomes are incontrovertible, multipartite entities that result from ecological, evolutionary and genetic processes at varying levels. They are not restricted to one special process but constitute a wider vocabulary and framework for host biology in light of the microbiome.

Gardner (2015) recently developed a model of a ‘Genetical Theory of Multilevel Selection, which is a thoughtfully developed, but flawed model. The model's flaws appear to be symptomatic of common misunderstandings of the multi level selection (MLS) literature and the recent quantitative genetic literature. I use Gardner's model as a guide for highlighting how the MLS literature can address the misconceptions found in his model, and the kin selection literature in general. I discuss research on the efficacy of group selection, the roll of indirect genetic effects in affecting the response to selection and the heritability of group‐level traits. I also discuss why the Price multilevel partition should not be used to partition MLS, and why contextual analysis and, by association, direct fitness are appropriate for partitioning MLS. Finally, I discuss conceptual issues around questions concerning the level at which fitness is measured, the units of selection, and I present a brief outline of a model of selection in class‐structured populations. I argue that the results derived from the MLS research tradition can inform kin selection research and models, and provide insights that will allow researchers to avoid conceptual flaws such as those seen in the Gardner model.

Two common features of long-term selection experiments are that, first, there is typically no evidence for selection limits due to exhaustion of genetic variation, and second, selection plateaus are frequently observed that last multiple generations before a response to selection is resumed. These features are usually attributed to the high mutation rates of quantitative traits, and the effects of linkage disequilibrium. Using previously published theoretical results and a simple deterministic model I explore the potential role of gene interaction in generating these patterns seen in the response to long-term selection experiments. I show that epistasis provides a pool of variation that can contribute to an extended response to selection, but that this extended response will, at least under some circumstances, result in intermediate selection plateaus.

When Hamilton defined the concept of inclusive fitness, he specifically was looking to define the fitness of an individual in terms of that individual's behavior, and the effects of its’ behavior on other related individuals. Although an intuitively attractive concept, issues of accounting for fitness, and correctly assigning it to the appropriate individual make this approach difficult to implement. The direct fitness approach has been suggested as a means of modeling kin selection while avoiding these issues. Whereas Hamilton's inclusive fitness approach assigns to the focal individual the fitness effects of its behavior on other related individuals, the direct fitness approach assigns the fitness effects of other actors to the focal individual. Contextual analysis was independently developed as a quantitative genetic approach for measuring multilevel selection in natural populations. Although the direct fitness approach and contextual analysis come from very different traditions, both methods rely on the same underlying equation, with the primary difference between the two approaches being that the direct fitness approach uses fitness optimization modeling, whereas with contextual analysis, the same equation is used to solve for the change in fitness associated with a change in phenotype when the population is away from the optimal phenotype.

A metacommunity can be defined as a set of communities that are linked by migration, and extinction and recolonization. In metacommunities, evolution can occur not only by processes that occur within communities such as drift and individual selection, but also by among-community processes, such as divergent selection owing to random differences among communities in species composition, and group and community-level selection. The effect of these among-community-level processes depends on the pattern of migration among communities. Migrating units may be individuals (migrant pool model), groups of individuals (single-species propagule pool model) or multi-species associations (multi-species propagule pool model). The most interesting case is the multi-species propagule pool model. Although this pattern of migration may a priori seem rare, it becomes more plausible in small well-defined ‘communities’ such as symbiotic associations between two or a few species. Theoretical models and experimental studies show that community selection is potentially an effective evolutionary force. Such evolution can occur either through genetic changes within species or through changes in the species composition of the communities. Although laboratory studies show that community selection can be important, little is known about how important it is in natural populations.

Understanding mechanisms for the evolution of barriers to gene flow within interbreeding populations continues to be a topic of great interest among evolutionary theorists. In this work, simulated evolving diploid populations illustrate how mild underdominance (heterozygote disadvantage) can be easily introduced at multiple loci in interbreeding populations through simultaneous or sequential mutational events at individual loci, by means of directional selection and simple forms of epistasis (non-linear gene-gene interactions). It is then shown how multiscale interactions (within-locus, between-locus, and between-individual) can cause interbreeding populations with multiple underdominant loci to self-organize into clusters of compatible genotypes, in some circumstances resulting in the emergence of reproductively isolated species. If external barriers to gene flow are also present, these can have a stabilizing effect on cluster boundaries and help to maintain underdominant polymorphisms, even when homozygotes have differential fitness. It is concluded that multiscale interactions can potentially help to maintain underdominant polymorphisms and may contribute to speciation events.

Previous work has shown that speciation can result from the self-organized accumulation of multiple mildly underdominant (nearly neutral) loci in a continuous population, when mating is spatially localized. In contrast, when mating is panmictic, underdominance is quickly eliminated and the population always converges on a single genotype, as predicted by mean-field approximations. The focus of this work is to examine the sensitivity of self-organizing speciation to the assumption of purely localized interactions. We alter the interaction topology from nearest neighbor interactions to panmictic interactions in two ways: (i) by increasing the size of the contiguous mating neighborhoods and (ii) by allowing for long-distance dispersal of individuals with increasing probability. Our results show self-organized speciation to be robust to mating neighborhood sizes significantly larger than nearest neighbor interactions and to probabilities of long-distance dispersal that fall well into the range of so called "small-world" interaction topologies