Model Systems for Environmental Signaling1

Integrative and Comparative Biology, Sep 2005 by Blackstone, Neil W, Bridge, Diane M

SYNOPSIS.

Studies of environmental signaling in animals have focused primarily on organisms with relatively constrained responses, both temporally and phenotypically. In this regard, existing model animals (e.g., "worms and flies") are particularly extreme. Such animals have relatively little capacity to alter their morphology in response to environmental signals. Hence, they exhibit little phenotypic plasticity. On the other hand, basal metazoans exhibit relatively unconstrained responses to environmental signals and may thus provide more general insight, insofar as these constraints are likely traits derived during animal evolution. Such enhanced phenotypic plasticity may result from greater sensitivity to environmental signals, or greater abundance of suitable target cells, or both. Examination of what is known of the components of environmental signaling pathways in cnidarians reveals many similarities to well-studied model animals. In addition to these elements, however, macroscopic basal metazoans (e.g., sponges and cnidarians) typically exhibit a system-level capability for integrating environmental information. In cnidarians, the gastrovascular system acts in this fashion, generating local patterns of signaling (e.g., pressure, shear, and reactive oxygen species) via its organism-wide functioning. Contractile regions of tissue containing concentrations of mitochondrion-rich, epitheliomuscular cells may be particularly important in this regard, serving in both a functional and a signaling context. While the evolution of animal circulatory systems is usually considered in terms of alleviating surface-to-volume constraints, such systems also have the advantage of enhancing the capacity of larger organisms to respond quickly and efficiently to environmental signals. More general features of animals that correlate with relatively unconstrained responses to environmental signals (e.g., active stem cells at all stages of the life cycle) are also enumerated and discussed.

INTRODUCTION: CONSTRAINED AND UNCONSTRAINED PLASTICITY

In modern biology it is widely accepted that several independent laboratories focusing on a particular "model organism" can make significant progress (e.g., Alberts et al., 2002). This approach has been repeatedly validated, as for instance by the Nobel Prize award in 2002 for work on Caenorhabditis elegans (Check, 2002, p. 549):

Some scientists also see a larger significance to this year's Nobel, especially when combined with the 1995 Nobel for work in the fruitfly and the 2001 prize, which rewarded groundbreaking work in yeast. 'These awards are a recognition that you can make major advances in medicine by studying genetically tractable model organisms,' says Gerald Rubin, a vice-president at the Howard Hughes Medical Institute in Chevy Chase, Maryland.

Nevertheless, it is unlikely that "worms and flies" are sufficient for understanding animal diversity. Are there general traits of animals that cannot be well studied using these two model organisms? In this context, we suggest that one such trait is environmental signaling, here considered primarily in terms of developmental pathways influenced by cues that initiate outside the organism. In particular, we focus on pathways that have a measurable morphological outcome. The nature of the interaction between environmental signaling and development can be best understood in animals that differ strikingly from conventional model organisms (Bolker, 1995).

In studies of development, the effect of environmental signaling on organismal phenotypes is usually termed phenotypic plasticity. Considerable interest in this topic is evident (Schlichting and Pigliucci, 1998; Pigliucci, 2001; West-Eberhard, 2003). The role of such environmental signaling is likely commensurate with several organismal features related to longevity. For instance, short-lived animals typically exhibit only a brief window in which development will respond to environmental signals, since the period of development itself is brief. Appropriate environmental signals during this period may produce a response. The response itself is somewhat constrained, e.g., different body or limb size and shape, but not more body axes. Subsequently that response usually becomes fixed. The organism may or may not survive and reproduce, but typically no further effects of environmental signaling will be seen. Such animals notably include rotifers (Gilbert, 2003), crustaceans such as Daphnia (Tollrian and Dodson, 1999), and many insects, including the castes of social insects (Nijhout, 2003).

For instance, in the rotifer Asplanchna sieboldi, the amount of dietary α-tocopherol (vitamin E, an anti-oxidant) determines the morphotype that will develop. Morphotypes differ in body size and shape and type of offspring produced (e.g., amictic versus mictic). Vitamin E exerts its primary influence on embryos when they are developing in utero. While some effects can be seen even at the late stages of embryogenesis, no effects of tocopherol treatment are seen during postnatal development (Gilbert, 1980). Insects show similar kinds of plasticity, e.g., in butterfly polyphenisms related to wing pattern, the environment-sensitive period occurs sometime during larval life (Nijhout, 2003). Subsequent to the metamorphic molt, no further change occurs. In Daphnia, some phenotypic responses are irreversible (e.g., body size), while others can be reversed over the course of several molts (e.g., neckteeth). The reversible traits are usually minor relative to the overall morphology and occur when the within-generation variation in the environment is high (Tollrian and Dodson, 1999).