Multilevel and kin selection in a connected world.

Wild et al. argue that the evolution of reduced virulence can be understood from the perspective of inclusive fitness, obviating the need to evoke group selection as a contributing causal factor. Although they acknowledge the mathematical equivalence of the inclusive fitness and multilevel selection approaches, they conclude that reduced virulence can be viewed entirely as an individual-level adaptation by the parasite. Here we show that their model is a well-known special case of the more general theory of multilevel selection, and that the cause of reduced virulence resides in the opposition of two processes: within-group and among-group selection. This distinction is important in light of the current controversy among evolutionary biologists in which some continue to affirm that natural selection centres only and always at the level of the individual organism or gene, despite mathematical demonstrations that evolutionary dynamics must be described by selection at various levels in the hierarchy of biological organization.

Isolation-by-distance and outbreeding depression are sufficient to drive parapatric speciation in the absence of environmental influences.

A commonly held view in evolutionary biology is that speciation (the emergence of genetically distinct and reproductively incompatible subpopulations) is driven by external environmental constraints, such as localized barriers to dispersal or habitat-based variation in selection pressures. We have developed a spatially explicit model of a biological population to study the emergence of spatial and temporal patterns of genetic diversity in the absence of predetermined subpopulation boundaries. We propose a 2-D cellular automata model showing that an initially homogeneous population might spontaneously subdivide into reproductively incompatible species through sheer isolation-by-distance when the viability of offspring decreases as the genomes of parental gametes become increasingly different. This simple implementation of the Dobzhansky-Muller model provides the basis for assessing the process and completion of speciation, which is deemed to occur when there is complete postzygotic isolation between two subpopulations. The model shows an inherent tendency toward spatial self-organization, as has been the case with other spatially explicit models of evolution. A well-mixed version of the model exhibits a relatively stable and unimodal distribution of genetic differences as has been shown with previous models. A much more interesting pattern of temporal waves, however, emerges when the dispersal of individuals is limited to short distances. Each wave represents a subset of comparisons between members of emergent subpopulations diverging from one another, and a subset of these divergences proceeds to the point of speciation. The long-term persistence of diverging subpopulations is the essence of speciation in biological populations, so the rhythmic diversity waves that we have observed suggest an inherent disposition for a population experiencing isolation-by-distance to generate new species.

On the thermodynamics of multilevel evolution.

Biodiversity is hierarchically structured both phylogenetically and functionally. Phylogenetic hierarchy is understood as a product of branching organic evolution as described by Darwin. Ecosystem biologists understand some aspects of functional hierarchy, such as food web architecture, as a product of evolutionary ecology; but functional hierarchy extends to much lower scales of organization than those studied by ecologists. We argue that the more general use of the term "evolution" employed by physicists and applied to non-living systems connects directly to the narrow biological meaning. Physical evolution is best understood as a thermodynamic phenomenon, and this perspective comfortably includes all of biological evolution. We suggest four dynamical factors that build on each other in a hierarchical fashion and set the stage for the Darwinian evolution of biological systems: (1) the entropic erosion of structure; (2) the construction of dissipative systems; (3) the reproduction of growing systems and (4) the historical memory accrued to populations of reproductive agents by the acquisition of hereditary mechanisms. A particular level of evolution can underpin the emergence of higher levels, but evolutionary processes persist at each level in the hierarchy. We also argue that particular evolutionary processes can occur at any level of the hierarchy where they are not obstructed by material constraints. This theoretical framework provides an extensive basis for understanding natural selection as a multilevel process. The extensive literature on thermodynamics in turn provides an important advantage to this perspective on the evolution of higher levels of organization, such as the evolution of altruism that can accompany the emergence of social organization.