To Know Behavior Is to Know Ecology and Physiology: Integration and the Flexible Phenotype

Within most multicellular species, it is variation within individuals in how the genome is expressed, not variation between individuals in the genome itself that produces the larger, more rapidly induced phenotypic variability. For example, in many temperate-zone bird species, the testes increase in size by ,100-fold over the course of a few weeks with the annual onset of the breeding season, a rate and magnitude of change within individuals that vastly exceeds the variation between individuals of the same species examined at the same stage of breeding. Feeding in some snakes elicits a change in digestive physiology and morphology that can include a doubling in liver, pancreas, and intestine mass and changes in stomach pH from 7–8 to 1–2, all within a week or so. Massive phenotypic variation. Zero genomic variation. These examples of phenotypic change are impressive in their magnitude as well as their speed, both of which influence the accessibility of selection. But these rates of change are relatively modest compared to the speed with which behavior can drive phenotypic change in animals. Behavior, as a field of study, has provided a perspective on phenotypic variation that few other disciplines, including epigenetics, can match, yet it has been through its integration with other levels of biological organization that has enabled the most insight. Just as architects consider both the surrounding physical environment as well as the eventual occupants in designing a building, behaviorists must consider both the ecological context and the developmental and physiological mechanisms that give rise to the behavior. As Niko Tinbergen suggested in 1963, behavior cannot be completely understood in the absence of understanding the forces that ultimately and proximately influence it, and it is therefore no wonder why behavioral research that integrates across multiple levels of biological organization has been so well received by the larger biological research community in recent times. The integration of multiple levels of biological organization combined with the importance of intra-individual phenotypic flexibility together serve as general themes throughout The Flexible Phenotype: A BodyCentred Integration of Ecology, Physiology, and Behaviour, a new book by Theunis Piersma and Jan A. van Gils. Piersma and van Gils take the reader through a loose history of their research program on the migration stop-over ecology, behavior, and physiology of the red knot (Calidris canutus), a migratory shorebird that has served as the foundation for their long-time collaboration. Although they load their story with examples and anecdotes from numerous other species, it is primarily the focus on the red knot that has enabled these authors to understand not only migratory stopover biology, but more generally behavior, ecology, and digestive physiology as a whole. The writing style is more conversational than that to which we are typically accustomed as readers of the scientific literature. But beneath such whimsical section titles as ‘‘Thermometers Do Not Measure Feelings’’ and ‘‘It Takes Guts to Eat Shellfish’’ is a foundation of scientific rigor. Part I of the book, ‘‘Basics of Organismal Design,’’ details the principles of water, heat, nutrient, and energy balance and explores the concept of symmorphosis, which posits that organisms are economically designed. Among the several intriguing ideas discussed in this section was one on the evolution of endothermy raised by Marcel Laassen and Bart Nolet in 2008. The adaptive basis for the evolution of endothermy has confounded researchers for decades, but, over the years, many converged on the idea that the elevated activity levels enabled by endothermy allowed better exploitation of relatively less active herbivores as a food resource. In other words, endothermic carnivores could more easily prey on herbivores. Taking an integrative approach by combining digestive physiology with foraging ecology, Laassen and Nolet hypothesized that endothermy evolved as a mechanism for burning the excess carbon consumed as part of a primarily herbivorous diet. Thus, endothermy may have first evolved in herbivores, not carnivores. Although researchers are sure to debate the evolutionary origins of endothermy for years to come, the utility of an integrative approach in this example was clear. Part II, ‘‘Adding Environment,’’ begins by discussing the relationships between