New Frontiers for Organismal Biology

Articles New Frontiers for Organismal Biology Understanding how complex organisms function as integrated units that constantly interact with their environment is a long-standing challenge in biology. To address this challenge, organismal biology reveals general organizing principles of physiological systems and behavior—in particular, in complex multicellular animals. Organismal biology also focuses on the role of individual variability in the evolutionary maintenance of diversity. To broadly advance these frontiers, cross-compatibility of experimental designs, methodological approaches, and data interpretation pipelines represents a key prerequisite. It is now possible to rapidly and systematically analyze complete genomes to elucidate genetic variation associated with traits and conditions that define individuals, populations, and species. However, genetic variation alone does not explain the varied individual physiology and behavior of complex organisms. We propose that such emergent properties of complex organisms can best be explained through a renewed emphasis on the context and life-history dependence of individual phenotypes to complement genetic data. Keywords: life history, phenotype, evolution, individuality, gene–environment interaction T he organism is the central unit for integration of both of the major determinants of biological form and function—genes and the environment (Lewontin 2000). However, over the past several decades, the focus of bio logy has shifted considerably to studying genes rather than organisms by moving in two directions simultaneously. Moving outward from the organism toward broadscale evolutionary issues, the synthesis of Mendelian genetics with Darwinian theory led to a creative focus on mathematics, modeling, and theoretical approaches, giving birth to population and quantitative genetics. Moving inward from the organism toward cellular and molecular biology, reductionist experimental approaches based on DNA technologies allowed the experimental dissection of cause–effect relationships between individual genes and their contribution to cellular and higher-level structure and function. These two movements resulted in many of the monumental discoveries and advances that define the current state of biology. However, they also led to an eclipse of the organism by the gene as the fundamental unit of biology. A focus on the gene will continue to be a major pillar of biology. In addition, the two broad gene-oriented lines of study outlined above, together with technological advances, have generated extensive fundamental knowledge that now has us superbly positioned for “returning to the organism” (Stillman et al. 2011). The challenge is to extend, integrate, and exploit the insights from “outward” and “inward” gene-oriented biology to develop a deeper understanding of individual organisms’ higher-order emergent characteristics, such as epigenetic mechanisms and complex physiological and behavioral traits, including intelligence. For instance, we need to better understand how individual variation in complex physiological and behavioral characteristics or traits influences ecological and evolutionary processes (Autumn et al. 2002, Gerhart and Kirschner 2007). Facing this broad challenge requires cross-fertilization and integration across the traditionally disparate fields of biology, including developmental biology, physiology, microbiology, behavioral biology, neuroscience, phylogenetics, and eco logy, and also requires the application of computationally intensive technologies to the emergent traits of the organism (Ungerer et al. 2008). These disciplines are already developing stronger bonds among one another because of their collective growing appreciation of the importance of the individual organism as a fundamental unit of study (Wake 2008). BioScience 63: 464–471. ISSN 0006-3568, electronic ISSN 1525-3244. © 2013 by American Institute of Biological Sciences. All rights reserved. Request permission to photocopy or reproduce article content at the University of California Press’s Rights and Permissions Web site at www.ucpressjournals.com/ reprintinfo.asp. doi:10.1525/bio.2013.63.6.8 464 BioScience • June 2013 / Vol. 63 No. 6 www.biosciencemag.org Dietmar Kültz, David F. Clayton, Gene E. Robinson, Craig Albertson, Hannah V. Carey, Molly E. Cummings, Ken Dewar, Scott V. Edwards, Hans A. Hofmann, Louis J. Gross, Joel G. Kingsolver, Michael J. Meaney, Barney A. Schlinger, Alexander W. Shingleton, Marla B. Sokolowski, George N. Somero, Daniel C. Stanzione, and Anne E. Todgham Articles Context dependence of organismal life-history trajectories Predicting how organisms will respond to adversity and adapt to environmental change is one of the overarching ambitions of contemporary biology, spanning both the www.biosciencemag.org applied and the theoretical domains. An urgent need in the context of global change, including climate shifts, human disturbance, acute environmental disasters, and invasive species, is to gain an understanding of integrated organismal responses to environmental change on very different timescales (e.g., minutes to hours, within an organism’s life span, or spanning multiple generations). More knowledge is needed on how organisms respond to acute, catastrophic, and extreme environmental events, including events such as tsunamis, earthquakes, volcanic eruptions, hurricanes, floods, and extreme thermal events. Such acute events are predicted to increase in frequency as a result of climate change and anthropogenic pollution of Earth’s atmosphere and oceans (van Aalst 2006, Yasuhara et al. 2011). Biological responses to acute environmental change are based on molecular, physiological, and behavioral mechanisms that rapidly confer plasticity to organismal phenotypes in order to maximize their coping ability under those conditions (Kültz 2005, Wingfield 2012). A central question concerns the determinants of plasticity during changing environmental and social circumstances—that is, to what extent prior life-history experiences and exposures relative to genetic factors influence coping ability. Arguably, the best context for such comparative biological inquiry is the individual organism (figure 1). Comparative analyses of how individuals respond to environmental perturbation and social challenges are also of interest in the context of evolutionary medicine (Stearns 2012) and with regard to an organism’s microbial symbionts, which have coevolved in close association with their hosts Figure 1. The three principal factors defining organismal phenotypes are the genotype of the individual, the environment in which the individual is embedded, and the life history experienced by the individual. The life history represents the sequence of environmental exposures during the course of the individual’s life—in particular, during early development—which are recorded as cellular and higher forms of memory. Organisms vary (...truncated)