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Onetouch 4.0 Sanned Documents Evolution, 48(2), 1994, pp. 287-296 EVOLUTIONARY SHIFTS IN THE SPECTRAL PROPERTIES OF SPIDER SILKS CATHERINE L. CRAIG,' GARY D. BERNARD,2 AND JONATHAN A. CODDINGTON3 ' Department of Biology, Osborn Memorial Laboratories, Yale University. New Haven, Connecticut 06511 2Department of Electrical Engineering, University of Washington, Seattle, Washington 98195 ^Department of Entomology, Smithsonian Institution, 105 NHB, 10th and Constitution Avenue, Washington, D.C. 20560 Abstract. • We measured the reflectance properties of unpigmented silks spun by a systematic array of primitive (Deinopoidea) and derived (Araneoidea) aerial, web-spinning spiders, as well as silks spun by Araneomorphae and Mygalomorphae spiders that do not spin aerial webs. Our data show that all of the primitive aerial web spinners produce catching silks with a spectral peak in the ultraviolet (UV), and cladistic analysis suggests that high UV reflection is the primitive character state for silk spectral properties. In contrast, all of the derived aerial web spinners produce silks that are spectrally flat or characterized by reduced reflectance in the UV. Correlated with the evolution of these catching silks is a 37-fold increase in species number and apparent habitat expansion. This suggests that the unique silk proteins spun by the araneoids have been important to their ecological and evolutionary diversity. Key words.• Spectral properties, spiders, spider silks. Received April 2, 1991. Accepted May 6, 1993. One basis of evolutionary change is the aerial web-spinning spiders, in addition to silks achievement of an adaptation or complex of ad- spun by all other spider species, yet to be ex- aptations that allows species to make better use plored. of resources than their ancestors (Wright 1978). We propose that if the physical properties of Numerous examples in the literature illustrate silk proteins have been important to spider spe- how molecular variations in proteins, shaped by ciation and the evolution of spider prey-capture natural selection, have allowed organisms to methods, then silks spun by phylogenetically adapt to diverse habitats or microenvironments primitive and phylogenetically derived, aerial, (reviewed in Gillespie 1991). Silks, a diverse web-spinning spiders will differ systematically. group of crystalline proteins spun by all spiders, We tested this hypothesis by comparing the spec- may be an example of a molecule that has been tral properties of unpigmented silks spun by 16 fundamental to the evolution of a predator's for- species of spiders in the superfamilies Deino- aging ecology. poidea and Araneoidea. For outgroup compar- Although it has been suggested that the chem- ison, we also examined the spectral properties of ical composition of silks spun by spiders is much silks spun by five spiders that spin sheet webs less variable than that of silks produced by larval and the retreat silks of three nonweb-spinning insects (Rudall and Kenchington 1971), almost spiders. all research on the molecular, structural, and me- MATERIALS AND METHODS chanical properties of spider silk has been com- pleted on the support and viscid threads spun by Spiders from Which Silks Were Sampled fewer than 15 species of orb spinners (Lucas et Silks were collected from spiders in the in- al. 1955;Zemlin 1968; Denny 1976; Wainwright fraorders Mygalomorphae and Araneomorphae. et al. 1976; Work 1977, 1981, 1985; Gosline et Silks sampled from Mygalomorphae include al. 1984; Craig 1987; Vollrath and Edmonds those spun by Aphonopelma sp. (Theraphosi- 1989; Xu and Lewis 1990; Dong et al. 1991; dae), Ishnothele sp. (Dipluridae), and Hexurella Beckwith 1991; Hinman and Lewis 1992). How- sp. (Mecicobothriidae). Among the Araneomor- ever, the orb-spinning spiders and their close rel- phae, the true spiders, we sampled silks spun by atives (the Araneoidea) include only about one- the most primitive spider in the group, Hypo- third of all described spiders. Thus, there exists chilus sp. (Hypochilidae; Platnick 1977), and silks a broad diversity in the types of silks spun by spun by a variety of more derived spiders in- 287 ) 1994 The Society for the Study of Evolution. All rights reserved. 288 CATHERINE L. CRAIG ET AL. eluding those in the families Eresidae (Stegody- Silks were collected on notched cards (Craig phus sp.), Diguetidae (Diguetia), Salticidae 1987) from the catching surface of sheet webs, (Phiddipus otiosus), Lycosidae {Sossipus sp.), and the catching threads of three-dimensional space Filistatidae (Kukulcania sp.). webs, the sticky spiral thread of webs spun by The spectral properties of silks spun by spiders aerial web weavers and from the retreat silks in the phylogenetically primitive, aerial web- spun by nonweb-spinning, hunting spiders. No spinning spiders, the Deinopoidea, and its sister data are currently available to indicate the degree taxon, the phylogenetically derived aerial web- of homology among these silks. spinning spiders, the Araneoidea (Coddington When silks are stressed their molecular con- 1986), were examined in more detail. Among the figuration may change (Dong et al. 1991), and Deinopoidea, silks were collected from webs spun hence their spectral properties as well. To stan- by Deinopis sp. (Deinopidae), Uloborus glomosus dardize our data, we collected silk at the tensions (Walckenaer), Hyptiotes cavatus (Hentz), Philo- at which the spiders laid them. In most cases, ponella tingena (Chamberlin and Ivie), and Mia- silks were collected and analyzed on the same grammopes animotus (Chickering) (Uloboridae). day they were produced. Among the Araneoidea, we measured the spec- Each sample was illuminated with a beam of tral properties of viscid silks produced by 11 monochromatic light and the light reflected back species in 10 genera of spiders and four families was measured in a UV-visible(350 nm-700 nm), (Araneidae, Tetragnathidae, Theridiosomatidae, incident-light microspectrophotometer. When the and Theridiidae). They include Argiope argen- spectral properties of sticky silks spun were mea- tata (Fabricius), Micrathena schreibersi (Perty), sured, the light was directed at one viscid droplet Mangora pia (Chamberlin and Ivie), Eustala an- (araneoid catching thread) or combed, silk puff astera (Walckenaer), Eustala sp., and Neoscona (deinopoid catching thread) and the thread on domiciliorum (Hentz) (Araneidae), Nephila cla- which they adhered. The microspectrophotom- vipes Linnaeus, Leucauge sp., Tetragnatha sp. eter is based on a Leitz Ortholux microscope with (Tetragnathidae), Epilineules globosus (O. Pick- MPV Pol-Opak illuminator, Nikon CF Fluor ard-Cambridge) (Theridiosomatidae), and Lat- 20 x/0.75 or 40x/0.85 objectives, andZeiss UV- rodectus mactans (Fabricius) (Theridiidae). projecti ve coupled to a Hammamatsu R928 pho- tomultiplier (Bernard 1982). The field stop of the Definition of Light Environments Epi-illuminator was reduced to illuminate a sin- We classified the light environments in which gle strand. The aperture stop was reduced to make the sampled spiders were foraging into three gen- the illumination as unidirectional as possible, and eral groups. Diurnal, nonforest habitats were the incident angle was made oblique to minimize classified as "bright." Diurnal, forest habitats were instrumental stray light. Light reflected from the classified as "dim," and nocturnal habitats were strand was collected over the full numerical ap- classified as "dark." erture of the microscope objective. The instru- mental baseline was calibrated with a National Silk Measurement Techniques Bureau of Standards SRM-20003D spectral re- Most spiders spin silks that are unpigmented flectance standard. and most silks appear flat white, translucent, or We measured the spectral properties of silks iridescent. These differences in the reflectance over a range of 350 nm to 700 nm at 10-nm properties of silks are apparent at casual obser- intervals. It is not possible to relate microspec- vation and suggest that silk proteins differ in their trophotometer absolute spectra to field absolute physical structure. To capture this range of vari- spectra. Therefore, the normalized spectral re- ation, we focused our analysis on quantifying silk flectance functions were calculated by dividing spectral variations spun by an array of phylo- the reflectance at each wavelength by the maxi- genetically primitive and derived spiders. Nev- mum reflectance for that sample. This allows us ertheless, to make sure that any variation in spec- to compare the shape of silk reflectance spectra tral properties of silks spun by individuals of the and the variation in reflectance as wavelength same species was minor relative to variations in changes. spectral properties of silks spun by different spe- cies, we collected and compared samples of sticky Phylogenetic Techniques silks spun by five adult Argiope argentata (Ara- To infer the ancestral character states for silk neidae). reflectance properties and foraging environ- SPECTRAL PROPERTIES OF SPIDER SILKS 289 CD CD CD T3 CD CD CD bl CD CD CD T3 "O F CD CD a CD CD 1c CD en o O CD CD CD CD CO CD CD CD ID -Q CD CD •a •Q T3 CD "O £= o O "CL <dJs D-S bl o D> ,T3 cz Q: A\ A• ^Jg. ^J|iJ| A* ul JJ'8o A ul JJ i^ •" CD ro Im -I luu I• a < • n • t LC Deinopoidea It t Araneoidea L^tZ Paleocribellatae Neocribellatae Light Environment Silk Relectance • Dark th High UV Mygalomorphae Araneomorphae Dim tZ Flat C Bright \L Low UV FIG. 1. Spectral properties of silks and spider foraging environments mapped onto a cladogram of the order Araneae
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