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concepts and principles from ecosystem, landscape, community and population ecology with those of the engineering sciences, particularly control theory. Before ecological engineering becomes a reality, however, ecologists must unify, s,implify and formalize their science. Ecology has been criticized for fuzzy concepts and preoccupation with description and explanation rather than prediction - with asking the question what and why, rather than how, when and where”. To become pragmatic engineers, ecologists must concern themselves more with prediction and less with retrospection, and must learn how, when and where to utilize other experts, as engineers do. They should recognize that ecodynamics is part of a much broader discipline - general systems theory, control theory and nonlinear dynamics5 and should have the humility to request the help of experts when faced with problems outside their area of expertise. Ecologists cannot be all things and, like engineers, should specialize in different areas - some in

ecothermodynamics, some in ecodynamics and some in ecodesign. They must all work together to build and maintain the global biosphere. They must also change the way the next generation of ecologists are educated. More emphasis must be placed on the predictive side of the science and more courses designed to teach the principles of control and stability. Finally, ecology must be drawn into the mainstream of those disciplines that have proven so useful to engineers. Control theory, in particular, should evolve to meet the needs and terminology of the ecologist.

References 1 Mitsch, W.]. and Jorgensen, SE. ( 1989) Ecological Engineering: An Introduction to Ecotechnology, lohn Wiley 2 Odum, H.T. (1971) Environment, Power, and Society, John Wiley 3 Blakney, R.B. (1953) Lao Tzu: The Way of Life, New American Library 4 Berger, 1.1.(1990) Environmental Restoration: Science and Strategies for Restoring the Earth, Island Press 5 Berryman, A.A. (1989) Bull. Ecol. Sot. Am. 70, 230-236

6 Berryman, A.A. ( I981 ) Population Systems: A Genera/ Introduction, Plenum Press 7 DeAngelis, D.L., Post, W.M. and Travis, C.C. (1986) Positive Feedback in Natural Systems, Springer-Verlag 8 Naveh, Z. (19901 Landscape Ecology: Theory and Application, Springer-Verlag 9 Gleik, 1. ( 1987) Chaos: Making a New Science, Penguin IO Logan, I.A. and Hain, F.P., eds (1991) Chaos and Insect Ecology, Virginia Experimental Station, Blacksburg I1 Peters, R.H. ( 1991) A Critique for Ecology, Cambridge University Press 12 Berryman, A.A. ( 1987) Bull. Ecol. Sot. Am. 68, 500-502 13 Berryman, A.A., Stenseth, N.C. and Isaev, A.S. (1987) Oecologia 71, 174-184 14 van den Bosch, R., Messenger, P.S. and Gutierrez, A.P. (1982) An Introduction to Biological Control, Plenum Press I5 Hawksworth, D.L., ed. (1991) The Biodiversity of Microorganisms and Invertebrates: Its Role in Sustainable Agriculture, CAB International I6 Thomas, M.B., Wratten, SD. and Sotherton, N.W. ( 199 I ) 1. Appl. Ecol. 28, 906-9 I 7 17 Harris, L.D. (1984) The Fragmented Forest; Island Biogeography Theory and the Preservation of Biotic Diversity, University of Chicago Press I.9 Berryman, A.A., Millstein, I.A. and Mason, R.R. (1990) in Population Dynamics of Forest Insects (Watt, A.D., Leather, S.R., Hunter, M.D. and Kidd, N.A.C., eds), pp. 369-380, Intercept

AerialWeb-Weaving Spiders: LinkingMolecularandOrganismal Processes in Evolution

evolution, their numerical diversity and the habitats in which they forage. For example, the phylogenetically primitive Deinopoidea forage only in dim light, and the superfamily includes just two families: the Deinopidae, comprising two genera and approximately 40 Aerial web-weuvi#gspiders display a wide variety of foraging behaviorsthat can be tied to the evolution of one family of proteins, the silks. In some cases,the physical struc- species, and the Uloboridae, comture and mechanicalpropertiesof silks alone determine the ecologyof spiders:the habitats prising 18 genera and 224 described in which they forage, the prey they capture and their subsequentreproductivesuccess. species (B.D. Opell, pers. commun.). Future studies that integrate researchon the physical structure of silks, the molecular In contrast, the phylogenetically genetics of silk synthesis and the foraging ecology of spiders in primitive and derived derived Araneoidea forage in both phylogenetic groups could reveal how molecular and organismal processesinteract in bright and dim light, and the superfamily is comprised of 10 families, evolution. 740 genera and 9810 species (NJ. Platnick, pers. commun.). There are two groups of orbDeinopoidea spin bluish silks Thus, the Araneoidea include brushed into fiber masses that web-weaving spiders, the primiapproximately 37 times more tive Deinopoidea and their sister entangle prey’. The Araneoidea species than the Deinopoidea and spin translucent silks of high group, the derived Araneoidea. The make use of a greater variety of web silks spun by spiders in strength and elasticity2”; the web’s catching thread is coated with a habitats. This suggests that the these two superfamilies differ. The evolution of silks with different viscid material to which insects spectral and mechanical properties adhere upon impact. allows spiders to forage in habitats The types of silk the spiders Catherine Craig is at the Department of Biology,Yale not available to their ancestors - an University, PO Box 6666,New Haven, CT0651I, USA. spin can be correlated with their

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physical extension of the coiled fiber. Using circular dichroism, infra-red spectrophotometry and X-ray diffraction, Dong et al.” suggest that silk elasticity is also affected by the presence of secondary, short-chain molecules. These molecules consist largely of the amino acid alanine and are interspersed in the B-sheet regions of individual polypeptide chains”. When a silk thread is in a relaxed state the alanine-rich protein domains are disordered, but when stretched, the regions become Molecularstructureand mechanical helical and ordered. The molecular propertiesof silks Silks are a diverse group of ordering that results from fiber crystalline proteins, known as fibroin extension, however, is reversible proteins, and are produced by a and the helical molecules return to variety of invertebrates. X-ray dif- a disordered state when the fiber is fraction studies in the 1950s and relaxed. Dong et al. propose that 1960sshowed that arthropods spin the B-crystalline regions give silks at least five different fibroin their high tensile strength, whereas proteins7. Insect silks are used the transitions of the a-helical primarily for protection. Although regions between ordered and disvarious insect larvae spin silks of ordered states confer elasticity. differing chemical compositions, Their unpublished preliminary data only one type of silk is produced by suggest that inelastic silks do a single individual. The best stud- not contain alanine-rich protein ied is the anti-parallel, B-pleated domains. This finding is supported by Gosline eta14, who found that the sheet protein spun by Bombyxmori, the domesticated silkworm. Such inelastic silks spun by silkworms are proteins are composed largely of more crystalline than the elastic the amino acids glycine, alanine and silks spun by spiders. serine, and are characterized by high tensile strengths8. Spiders, Molecularstructureand spectral however, produce up to nine propertiesof silk A recent survey of silk spectral different types of silk that are used for protection, foraging and properties reveals three types of patterns: silks that selectively reproduction9. The orb-web-spinning spiders reflect light or are characterized by spin the greatest diversity of silks. spectral peaks in the ultraviolet (LJV), Even within webs spun by single silks that are spectrally flat or that individuals, different components reflect light evenly across all are formed from different silks2.3e5,6.wavelengths, and silks that are For example, the viscid, catching silk characterized by a gap in the UV spun by Mangora pia (Araneoidea: where reflectance is weak (Fig. 1) Araneidae) is six times more elastic (C.L. Craig, G.D. Bernard and 1. than the web’s support or frame silk. Coddington, unpublished). Mapping the spectral properties Nevertheless, the breaking strength of the frame silk is an order of of silks onto a recent cladogram of magnitude greater than that of the the Araneae12illustrates how major viscid thread6. Silk elasticity and differences in silk spectra correlate tensile strength mustact together, to with phylogenetic patterns (Fig. I). allow spider webs to absorb the For example, the Mygalomorphae impact of intercepted prey, suggest- and the most primitive of the ing that silks with different mechan- Araneomorphae, Hypochilud3, proical properties are adapted to duce silks characterized by a different web functions5. spectral peak in the UV. Among the Vollrath and Edmondsl” have orb-web weavers, all spiders in the shown that portions of the web family Uloboridae (Deinopoidea) spiral thread lie coiled within each spin web silks characterized by a UV viscid droplet. Apparent thread spectral peak. All of the derived ‘elasticity’ is due, in part, to the aerial web weavers (Araneoidea), idea that could be tested through collaborative studies on the physical properties of silk proteins, the ecological and behavioral processes of spider foraging and detailed analysis of the spider genome. Here I outline our current understanding of silks and their function, and illustrate how future research on spider silk-producing systems could link evolutionary processes at the molecular and organismal levels.

however, spin silks characterized by reduced UV reflectance or silks that are spectrally flat. Thus, the ancestral character state for silk spectral properties is UV reflection and it is likely that primitive spiders were nocturnal. Furthermore, only the derived aerial web weavers produce viscid silks characterized by reduced UV reflectance (C.L. Craig et al., unpublished). Silk structureand the geneticsof silk production The complex nature of the mechanical functions of silk+” suggests that silks are multidomain molecules and, therefore, probably encoded by multiple exons (the coding regions of DNA). As yet, there are no published data on the comparative genetics of spider silk synthesis. However, collagen provides an example of a polymeric protein with a repetitive structure like silk14.Research on the collagen gene may provide clues for future studies on silks. Collagen proteins are produced exclusively by vertebrates and are a functional analogue of invertebrate silk+. Like silks, structural variations among the collagens are related to their different functional ro1es14.Although we have almost no data on the genetics of silk production (for most recent sequence data see Ref. 151,studies on the molecular genetics of collagen suggest two avenues through which studies on silks may be approached. At least five distinct types of collagen have been isolated from higher vertebrates. Except for their glycine residues, they show little sequence homology between different portions of the same collagen chain or between different collagens. Yamada et aLI determined the size and sequence of eight exons in the gene specifying (~2 collagen. Seven of the exons had 54 base pairs and one had 99 base pairs. The size and sequence of the intervening introns showed no homology except at their ends. In five of the seven introns examined, sequences at the 3’ ends were homologous and the first six bases at the 5’ end were identical. These results imply that the ancestral gene for a2 collagen arose by multiple duplications of a single genetic unit containing a 54 base pair 271

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Wavelength(nm) Fig. 1. Left: Three types of reflectance spectra of spider silks have been observed: spectrally flat (triangles), reflecting 70-100% of light across all wavelengths; spectra with an ultraviolet (UVI peak (stars) where 30% more light than adjacent regions is reflected across a region of about 30 nm; and spectra with a gap in the UV (circles). Right: The distributions of these silk types have been mapped onto the cladogram, as have the light intensities in which each group of spiders forage. Spiders that forage in nocturnal light environments (filled squares) and spiders that forage in dim, diurnal light environments (hatched squares) are found among all of the phylogeneticgroups studied. Web-spinning spiders that forage in bright,diurnal environments (open squares), however, are only found among the derived aerial web weavers in the superfamily Araneoidea. Cladistic analysis of the distribution of types of silks spun by spiders across the phylogenetic groups show that: both primitive and derived spiders spin silks that are spectrally flat; mygalomorph spiders the most primitive of the true spiders, Hypochilidae, and the primitive orb web weavers, Deinopoidea, all produce silks characterized by a spectral peak in the UV region; and none of the derived orb-web weavers spin silks that selectively reflect UV. Moreover, only the derived orb-web weavers. the Araneoidea. oroduce silks characterized by a gap in the ultraviolet or where reflectance is weak. From C.L. Craig, G.D.

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coding segment14. Differences in sequences within the exons are thought to have arisen by successive point mutations or by the addition or deletion of base pairs. Sequencing of the gene for dragline silk spun by Nephifa cbvipes (Araneoidea: Araneidae) shows that it also has a repetitive structure15.If future sequence studies include DNA analyses of the different types of silks produced by a single individual, it may be possible to determine the mechanisms by which the silk proteins evolved. For example, comparative data on gene sequences would reveal whether new silks resulted from the recombination of existing exon units or if point mutations split expressed genomic sequences, creating new 3’ and 5’ junctions. Moreover, comparison of the molecular sequences of homologous silks spun by primitive and derived aerial web weavers would reveal the genetic basis of their different physical properties, as well as degree of diversity. Studies of this nature would provide information on the mechanisms of molecular evolution and, in conjunction with ecological data, the interplay between molecular and organismal processes. 272

The significance of these rePrey capture at spider webs is a lationships lies in the apparent three-step process: insects must absence of a selective advantage encounter or contact webs1619,webs of orb architecture to low-energymust be able to absorb insect absorbing nets and the macroevolkinetic energy without breaking586 utionary trend to small spiders that and prey must adhere to the web build webs of alternative architecsurface long enough for the spider tural designs. Small, derived, web to subdue it20.Each of these events spinners are not constrained to build is dependent on the mechanical webs in the high-energy-absorbing properties of silkand the interaction design of an orb web. Derived between web materials and archi- spiders produce a variety of fiber tectural design5m6. For example, orb arrays and can make use of foraging webs that intercept insects with high sites and resources not available to kinetic energies (i.e. heavy or fast- the orb weavers2’. The reflectance properties of silks flying prey) are large, suspended under high tension and charac- also affect the foraging performterized by a radial to spiral-turn ratio ance of spiders. Silk reflectance greater than one. Their large num- properties, in particular color, are ber of support lines distribute insect usually determined by protein impact throughout the net. Due to molecular structure (for exception, their relatively dense construction, see Ref. 22) and silk color may high-energy-absorbing webs tend govern insect response to webs. to be highly visible. The visual systems of some Webs that can absorb only small insects are highly specialized amounts of insect kinetic energy and many insect behaviors are tend to have a radial to spiral- wavelength dependent, that is, turn ratio less than one. In these determined by narrowly defined cases the orb architecture con- bands of light23-25. If spiders tributes little to web energy absorp- spin colored silks that elicit a tion above the energy-absorbing wavelength-dependent response, properties of the silks. Hence, low- insects may be drawn to webs that energy-absorbing webs intercept would be recognized and avoided if small or slow-flying insects regard- spun from silks of different colors (C.L. Craig et al., unpublished). For less of web design21. Silk proteins and spider foraging ecology

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example, all insects display an open-space or UV attraction response. Webs spun from UVreflecting silks may be able to attract insects that are flying from closed to open space. Other insects, however, respond to a greater range of stimuli and forage for ephemeral and varying resources in a variety of light environments. These insects must be able to recognize, generalize and modify their search behavior as resource availability and light environment change. Thus, for these insects, at least some of their behaviors are not wavelength dependent and can be modified through leaming26. The primitive aerial web weavers produce UV-reflecting silks that attract prey but these spiders forage only at night or in dim sites. The derived aerial web weavers, however, spin webs composed of multiple types of silks and forage in all possible light habitats. For example, Argiope, a common garden spider, spins a spiral thread that appears blue-green to insects and thus its webs are difficult to see against background vegetation. Nevertheless, Argiope spp. decorate their webs with brightly colored, UV-reflecting silk designs. These patterns are similar to those found on flowers favored by pollinating insects27B28. The brightly colored web decorations attract insects but the catching portion of the web, the spiral, is difficult to see. The fact that all orb weavers do not spin decorated webs, however,

indicates there may be other undiscovered visual tricks by which spiders lure insects to their webs. Conclusion The functional specialization of silk production among the derived spiders, the shift in spectral properties of their silks and the correlated increases in species number suggest that silk proteins have played an important role in spider evolution. Silks are encoded by the spider genome and in some cases their physical and mechanical properties alone can determine spider ecology. The physical structure of the silkproteins, the molecular genetics of silk production and the effects of silkproteins on spider foraging performance represent one system in which the interplay between molecular and organismal processes in evolution can be explored. Acknowledgements I thank Cheryl Y. Hayashi for helpful discussions on this work and R. Weber for critically reviewing the manuscript. This work was supported by the National Science Foundation (BNS-9109468) and Yale University.

References I Opel], B.D. (1979) Bull. Mus. Comp. Zoo/. 148, 445-549 2 Denny, M. (19761 1. Exp. Biol. 65, 483-506 3 Denny, M.W. ( 1980) Sot. Exp. No/. Symp. 34, 247-272 4 Gosline, J.M., Denny, M. and Demont, M.E. (1984) Nature 309, 551-552 5 Gosline, I.M., Denny, M. and Demont, M.E. (1986) Endeavour 10, 37-43 6 Craig, C.L. (19871 Bio/. 1. Linn. Sot. 30,

135-162 7 Rudall, K.M. and Kenchington, W. (1971) Annu. Rev. Entomol. 16,73-96 8 Wainwright, S.A., Biggs, W.D., Currey, J.D. and Gosline, I.M. (19761 Mechanical Design in Organisms, Princeton University Press 9 Kovoor, I. ( 1987) in Ecophysiology of Spiders (Nentwlg, W., ed.), pp. 160-186, Springer-Verlag 10 Vollrath, F. and Edmonds, D.T. (19891 Nature 340, 305-307 II Dong, Z., Lewis, R.V. and Middaugh, C.R. I199 I ) Arch. Biochem. Biophys. 284, 53-57 I2 Coddington, I. and Levi, H.W. ( I99 I ) Annu. Rev. Ecol. Syst 22, 565-592 13 Platnick, NJ. (1977) Am. Mus. Novit. 2627, i-23 14 Yamada, Y. et al. (1980) Cell 22, 887-892 15 Xu, M. and Lewis, R.V. ( 1990) Proc. Nat/ Acad. Sci. USA 87, 7120-7124 16 Chacon, P. and Eberhard, W.G. (1980) Br. Arachnof. Sot. Bull. 5, 29-38 17 Rypstra, A. (1982) Oecologia 52, 3 1-36 18 Craig, C.L. ( 19881 Fun&. Ecol. 2, 277-282 I9 Craig, C.L. and Freeman, C.R. (1991) Behav. Ecol. Sociobiol. 29, 249-254 20 Nentwig, W. (19821 Oecologia 53, 412-417 21 Craig, CL. (1987) Am. Nat 129, 47-68 22 Holl, A. and Henze, M. (1988) in Europaisches Arachnologisches Colloquium: Comptes Rendus du Xlr?me Colloque D’Arachnologie (Haupt, I., ed.), p. 350, Technische Universitit Berlin 23 Menzel, R. (1985) in Experimental Behavioral Ecology and Sociobiology (Holldobler, B. and Lindauer, M., edsl, pp. 55-74, Sinauer Associates 24 Menzel, R. ( I9901 Co/or Vision in Flower Visiting Insects, Forschungszentrum liilich 25 Wehner, R. (1981 I in Comparative Physiology and Evolution of Vision in Invertebrates, II: Invertebrate Visual Centers and Behavior (Autrum, H., ed.), pp. 285-618, Springer-Verlag 26 Goldsmith, T.H. (1990) 0. Rev. Biol. 65, 281-322 27 Craig, C.L. and Bernard, G.D. (1990) Ecology 71, 616-623 28 Barth, F.G. (19851 Insects on Flowers: The Biology of a Partnership, Princeton University Press

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