Catherine L. Craig
Museum Associate
Museum of Comparative Zoology Laboratories
Office: (617) 496-8146
Home Fax: 617-642-0931
Home: (617) 893-5525
ccraig@oeb.harvard.edu



Research Interests

Correlating the evolution of a family of proteins or enzymes with suites of physiological adaptations has increased our understanding of how organisms adapt to diverse ecological regimes (1). In most cases, however, the translation of specific patterns of molecular variation into higher level evolutionary effects is masked by complicating intracellular, tissue or organ level interactions. Silk proteins and spider web-spinning behavior represent one system that by-passes these intra-organism filters allowing an integrated approach to understanding how the molecular evolution of a protein can affect and be directed by shifts in animal foraging behavior and ecology. My research links specific changes in protein composition and structure with shifts in animal behavior and ecology that have led to phyletic diversifications among the arnaeoids (2).

To achieve these goals I incorporate molecular, organismal and theoretical approaches. In light of the shared, common origins of insects and spiders (3, 4), I am interested in why spiders evolved to produce multiple types of proteins in multiple types of silk producing glands, while insects, subjected to similar selection pressures, did not. My previous studies have focused on identifying the selective forces that have affected the evolution of silk functional properties beyond baseline energetic and synthetic considerations. These include investigations of the physical properties of silks (5, 6, 7) and the ability of spiders to adjust them in response to controlled, environmental conditions (8). Through a series of laboratory experiments I have shown that some spiders selectively synthesize a cocktail of pigments that mask the natural reflectance properties of their silks in response to intensity and spectral distribution of their light environment. This work, done in conjunction with field experiments, has illustrated that the physical properties of silks affect insect perception of webs under different light and background conditions (9, 10, 11). Furthermore, field studies on freely-flying insects show that the evolution of spider web-spinning behavior and manipulation of silk reflectance properties affect spider foraging performance(10, 12, 13) as well as the ability of insects to see webs, to learn to avoid them, and to remember their locations (8, 9, 14, 15, 16). Thus shifts in web visibility, determined by spider spinning behavior, affect insect response to webs and subsequently the complex of prey on which spiders feed.

Recent comparisons of the molecular composition (17), structure (18, 19) and physical properties of silks spun by insects (2) and spiders (9) suggest that their structural differences may be anchored in the contrasting complex of resources on which herbivores and predators feed. These diffences may have been further magnified through selection for alternative, physical properties (2). For example, cocoon silks produced by herbivorous, Lepidoptera larvae are largely crystalline in composition (20), stiff (21), highly reflective (reviewed in 2) and comprised of glycine, alanine and serine (22). These properties make them similar in composition and structure to the capture silks produced by ancestral web-spinning spiders. In contrast, the capture silks produced by the more highly derived araneoid spiders are molecular composites containing both crystalline and amorphous protein domains (23, 24, 25), and characterized by reduced reflectance (9, 26) and high extensibility (7, 27) are comprised of the amino acids glycine, alanine and proline (17). To understand how the compositional differences among these highly expressed proteins evolved, it has proven important to address a fundamental problem of evolutionary biology, the biased retention of some amino acids yet selective rejection of others (contrasting views expressed in 28, 29). I have proposed that the baseline selective force leading to structural differences among proteins, and specifically silks produced by insects and spiders, reflects selection for reduced bioenergetic costs and biosynthetic complexity in the context of the differing resources that are available to them. Functional differences among the silks spun by insects and spiders are secondarily enhanced through selection.

To test this idea we have developed a method to quantitatively evaluate the cost and complexity of synthesizing proteins. We propose in the absence of constraint, highly expressed proteins will evolve towards reduced energetic and/or biosynthetic complexity (17). However, if evolving proteins enhance an essential function, then bioenergetic costs or synthetic complexity are not an important selective factor since need over-rides economics. We tested this idea on proteins produced by the closely related ColE1 and ColIa, plasmids harbored by the bacteria Escherichia coli (30). Comparing total protein ŇcostÓ as well as the cost of specific amino acid substitions across two protein lineages, we found that undifferentiated ColE1 colicin proteins were evolving towards reduced costs while the differentiated ColIA colicin proteins seem to have reached an economic minimum(31). Modifying and extending this model to analysis of silk production in insects and spiders suggests that the contrasting silk proteins produced by insects and spiders reflects a shift in the availability of the amino acids serine and proline. Proline, requiring significantly more ATP for an herbivore to produce than glycine, alanine or serine, it is found in appreciable quantities in the hemolymph of holometabolous insects (32), and hence readily available to predatory spiders. The incorporation of proline into the silk molecule correlates with increased extensibility, important to web interception capabiltiies, and decreased reflectance, important to web visiblity and hence insect avoidance to webs.


Future Research

To extend this analysis and achieve my broader goal of understanding of how the evolution of silks may be related to the phyletic diversity of aerial web-spinners requires a detailed, systematic template on which to test evolutionary hypotheses of specialized silk types and web-spinning behavior. I have begun to outline a molecular phylogeny of spiders in the genera Argiope and Nephila in conjunction with a focused study on the population structure of the species A. argentata and N. clavipes. These two spider species, distributed from southern Brazil to southern Florida and in habitats ranging from open grassland, to closed forest, desert and mangrove swamps, display specialized adaptations in silk use and structure that are demonstrated to affect the types of prey they capture. Hence, if variations in silk composition are important in spider species diversity, then it is reasonable to predict that spiders previously identified as A. argentata and N. clavipes species may actually include cryptic species whose evolutionary differences correlate with differences in the composition of their silks and web-spinning behavior. I have isolated and am using the CO1 gene to outline subspecies and subgroup levels of variation within Argiope and Nephila and the NADH-1 gene to explore population structure and divergence (33). Sequences from ITS1 and ITS2 will be used to identify cryptic species. While my initial studies are focussed on radiations of Argiope and Nephila in the Americans and Caribbean, I plan to compare their speciation patterns with the apparently much more complex speciation patterns of Argiope and Nephila in Asia and the Indo-Pacific. I hope to determine if speciation among these spiders is mediated by evolution of the composition and structure of silk protiens.

1. J. H. Gillespie, The Molecular Causes of Evolution (Oxford University Press, New York, 1992).
2. C. L. Craig, Annual Reviews of Entomology 42, 231-267 (1997).
3. G. Panganiban, Sebring, A. Nagy, L. Caroll, S., Science 270, 1363-1366 (1995).
4. J. Grenier, et al. Current Biology (1997).
5. C. L. Craig, Animal Behaviour 34, 54-68 .
6. C. L. Craig, Am. Nat. 129, 47-68 (1987).
7. C. L. Craig, Biol. J. Linn. Soc. 30, 135-162 (1987).
8. C. L. Craig, Behavioral Ecology and Sociobiology 35, 45-53 (1994).
9. C. L. Craig, G. D. Bernard, J. A. Coddington, Evolution 48, 287-296 (1994).
10. C. L. Craig, G. D. Bernard, Ecology 71, 616-623 (1990).
11. C. L. Craig, R. S. Weber, G. D. Bernard, The American Naturalist (1996).
12. C. L. Craig, K. Ebert, Functional Ecology 8, 616-620 (1994).
13. C. L. Craig, Funct. Ecol. 5, 649-654 (1991).
14. C. L. Craig, Anim. Behav. 39, 135-144 (1990).
15. C. L. Craig, C. F. Freeman, Behavioral Ecology and Sociobiology 29, 249-254 (1991).
16. C. L. Craig, Animal Behaviour 47, 1087-1099 (1994).
17. C. L. Craig, D. Kaplan, (in prog.).
18. A. Bram, C. I. BrŠnden, C. Craig, I. Snigireva, C. Riekel, J. Appl. Cryst. 30, 390-392 (1997).
19. C. L. Craig, C. Reikel, C. Branden, ((in progress)).
20. J. M. Gosline, M. E. Demont, M. Denny, Endeavour 10, 37-43 (1984).
21. M. W. Denny, in The Mechanical Properties of Biological Materials J. F. V. Vincent, J. D. Currey, Eds. (Society for Experimetal Biology, 1980), vol. Society for Experimental Biology
Symposium XXXIV, pp. 247-271.
22. K. M. Rudall, W. Kenchington, Annual Review of Entomology 16, 73-96 (1971).
23. J. M. Gosline, Demont, M.E., Nature 309, 551-552 (1984).
24. M. Xu, R. V. Lewis, Proceedings of the National Academy of Sciences U.S.A. 87, 7120 (1990).
25. A. H. Simmons, C. A. Michal, L. W. Jelinski, Science 271, 84-87 (1996).
26. C. L. Craig, Funct. Ecol. 2, 277-282 (1988).
27. M. W. Denny, J. Exp. Biology 65, 483-506 (1976).
28. M. Kimura, in Evolution of Genes and Proteins Sunderland, Ed. (Sinauer Associates, Sunderland,
1983) pp. 208-233.
29. R. C. Lewontin, The Genetic Basis of Evolutionary Change (Columbia University Press,
New York, 1965).
30. M. A. Riley, Y. Tan, J. Wang, Proc. Nat. Acad. Sci. 91, 11276-1128 (1994).
31. C. L. Craig, R. S. Weber, (in review).
32. D. W. Sutcliffe, Comp. Biochem. Physiol. 9, 121-135 (1963).
33. M. Hedin, Mol. Biol. Evol. 14, 309-324 (1997).

Biographical Information

    1997-1998 American Association of University Women, Fellow Museum Associate,
    1995-1997 Science Scholar, Fellow, Bunting Institute of Radcliffe College
    1995-1996 John Simon Guggenheim Fellow
    1991-1995 Associate Professor, Division of Ecology and Evolutionary Biology, Yale University
    1985-1991 Assistant Professor, Division of Ecology and Evolutionary Biology, Yale University
    1985 PhD, Section of Ecology and Systematics, Cornell University
    1976 MA, Zoology Department, University of California, Berkeley
    1973 AB, Program in Human Biology, Stanford University

Academic Honors

    1997 American Association of University Women, Fellow
    1996-1997 Fellow Mary Ingraham Bunting Institute, Radcliffe College, Harvard University
    1995 John Simon Guggenheim Fellow
    1995 Science Scholar, Mary Ingraham Bunting Institute
    1993 Alfred P. Sloan Foundation Faculty Fellowship
    1989 Morse Junior Faculty Fellowship, Yale College

Selected Publications

    Craig, C.L. 1997. Evolution of arthropod silks. Annual Reviews of Entomology. 42:231-67.

    Bram, A., C. I. Branden, C. Craig, I. Snigirova and C. Riekel. X-ray diffraction from a single fibre
    Craig, C. L., R.S. Weber and G.D. Bernard. 1996. Evolution of predator-prey systems:

    Craig, C.L. 1994. Limits to learning: effects of predator color and pattern on perception and

    Craig, C.L. 1994. Predator foraging behavior in response to perception and learning by its

    Craig, C.L. and K. Ebert. 1994. Color and pattern in predator-prey interactions: the bright

    Craig, C.L., G.D. Bernard and J.A. Coddington. 1994. Evolutionary shifts in the spectral