Evolvability and Robustness in Color Displays: Bridging the Gap between Theory and Data

Abstract

Evolution of diet-derived sexual ornaments-some of the most spectacular and diverse traits in the living world-highlights the gap between modern evolutionary theory and empirical data on the origin and inheritance of complex environment-dependent traits. Specifically, current theory offers little insight into how strong environmental contingency of diet-dependent color biosynthesis and environmental variability in precursor supply can be reconciled with extensive evolutionary elaboration, diversification, and convergence of diet-dependent displays among animal taxa. Moreover, biosynthetic pathways of diet-derived displays combine seemingly irreconcilable robustness, lability, and modularity to facilitate elaboration under variable environmental conditions. Here I show that an ontogenetic decrease in the predictability of an association between organismal and environmental components of color biosynthesis and the corresponding evolutionary transition from short-term epigenetic inheritance of peripheral biosynthetic components to genetic inheritance of the most reliable upstream components link the causes of developmental variation with the causes of inheritance in diet-derived displays. Using carotenoid-based colors as an empirical model, I outline general principles of a testable evolutionary framework of diversification and functional robustness of diet-derived displays, and suggest that such a framework provides insight into the foundational question of evolutionary biology-how to connect causes of withingeneration developmental variation with causes of amonggeneration and among-taxa variation and thus with causes of evolution?

Parental effects in ecology and evolution: mechanisms, processes and implications

“…The evolutionary dynamics of parental effects under parent-offspring conflict should depend on the relative costs and benefits of a particular set of strategies to the interacting individuals, the strength and consistency of selection on those strategies, and mechanistic aspects of interactions that influence whether or not one of the generations can impose their strategy on the other (Price 1998;Mü ller et al 2007;Uller 2008). This coevolution of parental and offspring traits results in the formation of phenotypic and genetic covariance between parents and offspring ( Wolf & Brodie 1998;Smiseth et al 2008), with the most consistent and recurrent configurations ultimately producing developmentally entrenched parental effects that are part of speciesspecific normal development (Badyaev 2007(Badyaev , 2008.…”

The role of behavior in evolution: a search for mechanism

“…Some types of behavioral shifts are more likely to meet this requirement than others. These include (1) developmental plasticity where different individuals within a population share a similar reaction norm and are exposed to the same environmental variation (West-Eberhard 1989Badyaev 2005Badyaev , 2007, (2) learning, but only if the learned trait is culturally transmitted (Irwin and Price 1999;ten Cate 2000;Price 2007), (3) selection, because it can shift the behavioral phenotype of the entire population (Duckworth and Badyaev 2007;Zuk et al 2006), and (4) a founder's effect because it can result in the reduction of a population's behavioral repertoire through the loss of both genetic and cultural diversity and this can influence the evolutionary trajectory of the founding population (Grant et al 2001). The diverse types of behavioral shifts listed above (see also Table 1) emphasize that the source of the behavioral shift (whether environmental or genetic) is less important than the proportion of the population experiencing the behavioral shift.…”

“…This idea, which has often been proposed as a mechanism of behavior as a driver of evolution (Wcislo 1989), emphasizes the role of behavioral plasticity in enabling colonizers of new environments to survive through phenotypic accommodation before adaptive evolution has time to occur (Baldwin 1896;West-Eberhard 2003). In this view, behavioral flexibility is thought to be crucial for enabling organisms to persist under novel environmental conditions (West-Eberhard 2003;Pigliucci et al 2006;Badyaev 2007). Ultimately, a behavioral shift in this context can lead to evolutionary change by enabling population persistence in a novel environment long enough for either stochastic processes or selection to produce divergence from the source population.…”

The beak of the other finch: coevolution of genetic covariance structure and developmental modularity during adaptive evolution

“…More important empirical considerations are the actual formation of the G matrix and historical changes in its dimensionality and, thus, the extent to which it can be used as a historical probe of population processes influencing a complex of traits. For example, are the lines of 'least genetic resistance ' (Bjö rklund 1996;Schluter 1996) the lines of greatest recurrence of organism -environment associations that reflect the evolved correspondence between developmental and functional integrations (Badyaev 2007) stabilized by genetic circuitry and accomplishing evolutionary integration (Baldwin 1902;Mü ller & Newman 2005)? Or are these lines the lines of 'the least selective resistance' (Arnold et al 2001) that delineate the direction of the least depleted additive genetic variance?…”