Mario Pineda-Krch

Costs and benefits of genetic heterogeneity within organisms

An increasing number of studies have recently detected within‐organism genetic heterogeneity suggesting that genetically homogeneous organisms may be rare. In this review, we examine the potential costs and benefits of such intraorganismal genetic heterogeneity (IGH) on the fitness of the individual. The costs of IGH include cancerous growth, parasitism, competitive interactions and developmental instability, all of which threaten the integrity of the individual while the potential benefits are increased genetic variability, size‐specific processes, and synergistic interactions between genetic variants. The particular cost or benefit of IGH in a specific case depends on the organism type and the origin of the IGH. While mosaicism easily arise by genetic changes in an individual, and will be the more common type of IGH, chimerism originates by the fusion of genetically distinct entities, and is expected to be substantially rare in most organisms. Potential conflicts and synergistic effects between different genetic lineages within an individual provide an interesting example for theoretical and empirical studies of multilevel selection.

Fluctuating population dynamics promotes the evolution of phenotypic plasticity.

Theoretical and empirical studies are showing evidence in support of evolutionary branching and sympatric speciation due to frequency‐dependent competition. However, phenotypic diversification due to underlying genetic diversification is only one possible evolutionary response to disruptive selection. Another potentially general response is phenotypic diversification in the form of phenotypic plasticity. It has been suggested that genetic variation is favored in stable environments, whereas phenotypic plasticity is favored in unstable and fluctuating environments. We investigate the “competition” between the processes of evolutionary branching and the evolution of phenotypic plasticity in a predator‐prey model that allows both processes to occur. In this model, environmental fluctuations can be caused by complicated population dynamics. We found that the evolution of phenotypic plasticity was generally more likely than evolutionary branching when the ecological dynamics exhibited pronounced predator‐prey cycles, whereas the opposite was true when the ecological dynamics was more stable. At intermediate levels of density cycling, trimorphisms with two specialist branches and a phenotypically plastic generalist branch sometimes occurred. Our theoretical results suggest that ecological dynamics and evolutionary dynamics can often be tightly linked and that an explicit consideration of population dynamics may be essential to explain the evolutionary dynamics of diversification in natural populations.

Challenging the genetically homogeneous individual

A growing number of empirical and theoretical studies suggest that naturally occurring intraorganismal genetic heterogeneity (IGH) may be more common than previously believed (for review see Pineda-Krch & Lehtilä, 2004). That the occurrence of genetically heterogeneous organisms in nature is of deep biological significance was recognized by Williams (1966) in his seminal Adaptation and Natural Selection. Nevertheless, the matter has received little attention in ecological and evolutionary research, and issues such as the frequency, the mechanisms and the potential significance of IGH remain largely unexplored. There seem to be two reasons for this omission and the general lines of argument can be summarized as follows: (i) it is important to maintain genetic homogeneity of an organism in order to avoid intraorganismal conflicts, hence IGH will be rare because there is strong selection against it and (ii) genetically heterogeneous organisms do not qualify as true gene vehicles and do not adhere to the predominantly accepted definition of individuality. Although the potential for IGH is acknowledged its significance is dismissed either because of its assumed rarity or the perceived difficulties in accommodating the idea within contemporary biological concepts. This line of reasoning is at least partially justified. That IGHs will often entail costs at the organism level is probably true, but currently we know little about the true distribution of effect, and as several of the commentaries show there is more to the story than what the statement suggests (Rinkevich, 2004; Santelices, 2004; Strassmann & Queller, 2004). It is also true that it would be difficult to accommodate IGH into the contemporary concept of individuality as, ever since Weismann, individuality has implied genetic homogeneity (Santelices, 1999). While several of the commentaries discuss the need for a revised individuality concept to accommodate situations such as IGH, Hutchings & Booth (2004) also appropriately point out that it is unlikely that any given definition will ever be applicable to all types of organisms. Indeed, the complexity of defining the individuality concept has been addressed on several occasions (Tuomi & Vuorisalo, 1989; Santelices, 1999). Nevertheless, a widely accepted conceptual revision has not yet occurred. Incorporating IGH into a revised concept of individuality will pose interesting challenges to theoretical and empirical research alike.