Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments

15. Experimental Approaches to Studying the Evolution of Animal Form: The Shape of Things to Come

419 15 EXPERIMENTAL APPROACHES TO STUDYING THE EVOLUTION OF ANIMAL FORM The Shape of Things to Come W. Anthony Frankino, Douglas J. Emlen, and Alexander W. Shingleton A systematic study of the effects of selecting for different kinds of proportional change in body parts would provide valuable evidence on the relative constancy or liability of the growth patterns which determine morphology. Indeed certain questions can be answered only this way. Selection is a useful tool which remains largely unexploited by students of physiology and development. Planned changes in growth and form can provide a wide range of differences for comparison and analysis. F. W. ROBERTSON (1962) MATHEMATICAL DESCRIPTIONS OF SHAPE VARIATION A Comment on Use of the Term Allometry DEVELOPMENT, SELECTION, AND THE EVOLUTION OF SCALING RELATIONSHIPS Theoretical Morphology: Putting Shape in Context Developmental Constraints and Scaling Relationship Evolution Drift, Natural Selection, and Scaling Relationship Evolution INCORPORATING DEVELOPMENT INTO STUDIES OF SHAPE EVOLUTION “Top-Down” Models for the Evolution of Animal Shape “Bottom-Up Models for the Evolution of Animal Shape EXPERIMENTAL EVOLUTION OF SCALING RELATIONSHIPS The Evolution of Eye Stalk Span–Body Size Scaling Relationships in Diopsid Flies The Evolution of Wing Scaling Relationships in Drosophila melanogaster The Evolution of the Wing Size–Body Size Allometry in Drosophila: Body Shape and Wing Loading The Evolution of Wing Dimension Allometry in Drosophila: Wing Shape The Evolution of Wing Scaling Relationships in the Little Brown Butterfly, Bicyclus anynana SPECIAL OPPORTUNITIES PROVIDED BY POLYMORPHIC SPECIES WITH NONLINEAR SCALING RELATIONSHIPS CONCLUSIONS AND FUTURE DIRECTIONS Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, edited by Theodore Garland, Jr., and Michael R. Rose. Copyright © by the Regents of the University of California. All rights of reproduction in any form reserved. Morphology most often evolves not through the appearance of new or “novel” traits, but through changes in the shape of existing structures (figure 15.1). Thompson presented shape variation as deformations in the dimensions and relative size of body parts (Thompson 1917); his approach captures differences in organismal shape across groups by 420 • A P P L I C A T I O N S FIGURE 15.1 Morphological diversity as generated through changes in shape and relative size of existing structures. Morphological variation among primates, shown in the first two rows, results from changes in the orbital fossa, teeth, maxilla and mandibles. Diversity in these same structures is even more extreme among other mammals, as shown in the bottom two rows. From left top to right, primate skulls are from an owl monkey, human, orangutan, gorilla, gelada baboon, and mandrill. Other mammal skulls belong to a walrus, babirusa, wombat, rough-toothed dolphin, beaver, and wolverine. Photography by David Littschwager with the California Academy of Sciences; all images used with permission. compressing, stretching, or bending a reference image, such as a common ancestral form or the mean shape calculated from lineages exhibiting shape variation (figure 15.2). This approach illustrates intuitively how disproportionate changes in dimensions across a generic, reference shape can produce both subtle variations on morphological themes and dramatically different, specialized morphologies. Such changes in animal shape are responsible for much of the gross-level morphological diversity in multicellular life, contributing to variation at all taxonomic levels: among orders, families, genera, species, and populations and even between sexes or among alternative morphotypes within a sex. Variation in shape is most obvious when morphological proportions reach extremes. Species that attain extraordinary, disproportionate trait sizes are often the focus of great attention by hobbyists, agriculturalists, and scientists. In an effort to produce attractive or more profitable forms, hobbyists and agriculturalists have used artificial selection to generate varieties with extreme—even grotesque—morphologies, such as many domestic breeds of pigeon or dog (Darwin 1859; figure 15.3A–B), and livestock with larger profitable parts (e.g., disproportionately large breast meat weights in domestic chickens; see Le Bihan-Duval et al. 1999). Not all extreme morphologies are artificially produced, however ; animals of many species naturally exhibit extreme trait proportions. Fiddler crabs, swordtail fish, spoonbills (figure 15.3C), stalk-eyed flies (see also Swallow et al. this volume), and horned beetles are just a few examples of organisms that derive their common names from exaggerations in the relative size of particular body parts. Such extreme morphologies often are associated with the evolution of highly derived behaviors or ecological specialization, and sexual selection in particular has yielded a tremendous diversity of extreme animal shapes (Darwin 1859...