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Has vertebrate chemesthesis been a selective agent in the evolution of arthropod chemical defenses?

Introduction

Arthropods are well known to use potent exocrine secretions, allomones, to repel predators (Eisner et al., 2005). The allomones are quite varied in chemical structure and include simple straight-chained hydrocarbons, alkenes, terpenes, alcohols, aldehydes, ketones, carboxylic acids, quinones, esters, lactones, phenols, and more (Blum, 1981; Whitman et al., 1990; Eisner et al., 2005). Most are small volatile molecules generally classed as repellents. The question we address in this paper is how arthropods have arrived at the specific compounds and blends of compounds that they use. Arthropod allomones are believed to affect free nerve endings in the epithelium, the common chemical sense, of their attackers (Eisner, 1970; Pasteels et al., 1983; Whitman et al., 1990), but has this sensitivity, later termed chemesthesis, in vertebrates and its specific receptivity molded the chemical weaponry of arthropods by acting as a specific target for their defenses?

The common chemical sense is mediated by chemesthetic nerve fibers originating in the trigeminal and dorsal root ganglia (Story and Cruz-Orengo, 2007). As such it is found in all of the major vertebrate lineages (Green et al., 1990). The trigeminal fibers innervate the skin of the face and the mucosa of the nasal and oral cavities and eyes. They terminate very near the surface of these tissues and are poly-modal; that is, they are sensitive to a variety of stimuli, including extreme temperatures and mechanical damage (Bryant and Silver, 2000). Most important in this context, they are considered the first line of defense against noxious chemicals (Finger et al., 2003; Frasnelli et al., 2004). Recent research has greatly expanded our knowledge of these chemical receptors and receptor mechanisms (Silver et al., 2006). Known receptors include the capsaicin-sensitive vanilloid receptor 1 (TRPV1) (Caterina et al., 1997; Dinh et al., 2003; Nakagawa and Hiura, 2006) and related receptors in the TRP family (Story and Cruz-Orengo, 2007), the acid-sensing ion channel (ASIC) (Ichikawa and Sugimoto, 2002), the purinergic receptor (P2X) (Spehr et al., 2004), and the nicotinic acetylcholine receptor (nACHR) (Alimohammadi and Silver, 2000).

Irritants of the trigeminal system can be studied by presenting airborne stimulants to the nasal mucosa while recording extracellularly from the ethmoid branch of the trigeminal nerve of the laboratory rat (Silver et al., 1990) or while measuring changes in breathing patterns (Alarie et al., 1998). More recently, less volatile stimulants have been perfused through the nasal cavity (Alimohammadi and Silver, 2005), and water-soluble stimulants have also been tested on specific protein receptors expressed in cell lines (see Caterina et al., 1997; Tominaga et al., 1998; Yang et al., 2003, for examples). A list of typical trigeminal stimulants based on such studies is shown in Table 1. The actual list of stimulants is likely much longer, and we believe that a database of arthropod allomones is an excellent place to search for candidates.

Multidimensional scaling has proven useful in describing olfactory landscapes and perceptual spaces; examples include the olfactory landscape pertinent to floral odors and their pollinators (Raguso, 2003) and the olfactory perceptual space of honeybees (Mamlouk et al., 2003). We use this method to explore the degree of overlap between known arthropod allomones and known trigeminal stimulants. A high degree of overlap can be construed as evidence that the trigeminal system and its inherent sensitivities have served to mold the suite of compounds arthropods use as allomones. Clustering in this multidimensional space represents groups of arthropod species that have arrived at the same or similar blends of chemicals. Clustering sometimes represents a phylogenetic signal, because related organisms tend to use similar compounds--as would be expected in organisms with a single common ancestor, common biochemical pathways, or common endosymbionts. More important for this study, clustering represents the convergent evolution of similarly effective solutions to the challenge of vertebrate predation. In this context, the target of the repellents may be the chemesthetic sense of vertebrates, and solutions cluster around trigeminal receptor sensitivity. Arthropod allomones can thus tell us a great deal about the characteristics of their molecular targets.

Materials and Methods

We used a compendium of allomonal compounds collected and published by Murray Blum in 1981 under the title Chemical Defenses of Arthropods. The information contained in this volume was supplemented by information from the Pherobase database available on the Web. We herein focus on relatively volatile allomones and their effects on terrestrial vertebrate predators. Our data set comprises 1216 arthropod species and 846 chemical compounds. We scored each species for presence or absence of each of the 846 compounds. Disconnected species (species with unique compounds or without a path connecting any of their compounds to the majority of the study species) were eliminated from the analysis. Only single representatives of multiple species with identical combinations of constituent compounds were included to avoid having multiple points occupy the same position in multidimensional space. The final ordination represents 348 species and species groups and 322 compounds.

All calculations were performed using the R programming language and environment (R Development Core Team, 2005). The Jaccard dissimilarity index was used to determine the distance between arthropod species in compound space (vegdist, package=vegan). Because the Jaccard index is metric (i.e., does not violate the triangle inequality) and is designed to handle presence-absence data, it was more appropriate to use in this study than the semi-metric Bray-Curtis dissimilarity index commonly used in community ecology (Clarke et al., 2006). The dissimilarity indices of species pairs having no compounds in common (~94%) were replaced with their flexible shortest path lengths, i.e., the number of steps through other species needed to link the compositions of the species pair being considered (stepacross, package=vegan) (Bradfield and Kenkel, 1987). The species were then mapped in multidimensional "compound space" and projected into two dimensions using Kruskal's non-metric multidimensional scaling (metaMDS, package=vegan). Multiple random starts demonstrated that the ordination results were independent of the order of data entry, enabled us to select the ordination with the lowest stress, and confirmed that the results discussed here were robust across all of the locally optimized ordinations. Whether the arthropod taxa represented significantly different samples of compound space (either in location or in spread) was tested using the multiple-response permutation procedure (mrpp, package=vegan, weight type=1), a multivariate nonparametric analog to an ANOVA that takes the variable taxon sizes into account.

Results

Figure 1 displays the results of our two-dimensional ordination with the lowest stress (22%) after 100 runs with random starts. Clusters of species using related allomones and/or blends of allomones are readily apparent. Colorcoded polygons (Fig. 2) represent the multidimensional compound space of single arthropod orders and illustrate the phylogenetic signal in the data; as expected, the signal is quite strong. The null hypothesis of no phylogenetic signal in the data was not supported by a multiple-response permutation procedure (P < 0.001). Additional tests showed that the Coleoptera, Dermaptera, Dictyoptera, Geophilomorpha, Hymenoptera, Juliformia, Lepidoptera, and Polydesmida had distributions in compound space significantly different from the mass of the data. The millipedes (Juliformia and Polydesmida), Heteroptera, Coleoptera, and Hymenoptera have invested heavily in volatile chemical defenses and are particularly well studied and therefore well represented in our data set. Especially important are clusters of species containing representatives of different orders of arthropods, because these represent convergence of the defensive use of particular chemistries.

[FIGURE 1 OMITTED]

Cluster A (Fig. 1) corresponds to arthropods that cluster in part because they utilize quinones--most notably 1,4-benzoquinone, 2-methyl-1,4-benzoquinone, and 2-methoxy-3-methyl-l,4-benzoquinone (Fig. 3). These and similar quinones are shared by disparate groups, including millipedes; cockroaches; tenebrionid, staphylinid, and carabid beetles; earwigs; and daddylonglegs (Opiliones). Compounds with ketone groups are frequently listed as trigeminal stimulants (Table 1). Examples include cyclohexanone, an industrial solvent known to be a respiratory irritant, and the plant products carvone, piperine, zingerone, and capsaicin and its analogs.

Species containing short-chained aldehydes, acids, and alcohols form a ring around cluster A. The right side of the ring is dominated by species with aldehydes. Specific examples (Fig. 3) include trans-2-hexenal, a pungent odorant released by some cockroaches and some Heteroptera; hexanal, secreted by some cockroaches and by coreid bugs; and trans-2-octenal, common in cockroaches and coreid and pentatomid bugs. Species utilizing benzaldehyde (Fig. 3), a common allomone frequently associated with cyanogenic activity, cluster separately (Fig. 1, cluster B). Benzaldehyde is shared by cyanogenic millipedes, centipedes, certain beetles, and Hymenoptera. Aldehydes are frequently listed as having trigeminal activity (Table 1 and Alarie et al, 1998).

[FIGURE 2 OMITTED]

The left side of the ring is dominated by species that contain short-chained acids, including acetic acid and isobutyric acid. These compounds are well represented in arthropod allomones and are frequently sprayed at assailants (Eisner et al., 2005). Carabid beetles, true bugs, larval Lepidoptera, and ants utilize acids that vary in carbon length from 1 to 12 carbons. Similar acids are also well represented in the list of trigeminal stimulants (Table 1 and Cometto-Muniz et al., 1998). A good example of a compound found in both lists is isobutyric acid. This compound is responsible for the memorable odor of the osmateria (extrusible defensive organs just behind the head) of papillionid butterfly larvae and many reduviid bugs (Fig. 3).

Aliphatic alcohols have some of the lowest thresholds as trigeminal stimulants. More than 60 different alcohols are present in the defensive secretions of arthropods, but frequently in low amounts (Blum, 1981). An example released by arthropods is 1-hexanol, a common component of coreid bug defenses. It is also found in some ants and occasionally in tenebrionid beetles (Fig. 3).

Cluster C represents species that contain straight-chained alkanes and alkenes. Examples are undecane and tridecane. These compounds are found in the exocrine secretions of a variety of Hymenoptera, Heteroptera, and beetles, and they are considered weak trigeminal irritants (Alarie et al., 1998). These compounds are also used as pheromones (Blum, 1981).

Discussion

Arthropods' allomones and trigeminal stimulants clearly overlap in multidimensional compound space. The convergence of multiple orders of arthropods on specific types of compounds argues that they have a common physiological target, i.e., the vertebrate trigeminal system. Specific classes of compounds are discussed below.

Since quinones play a role in the sclerotization of arthropod cuticle, they are readily available as exocrine substances (Chapman, 1998; Eisner et al., 2005). They are clearly extraordinarily effective repellents (Eisner et al., 2005). Given the sensitivity of the trigeminal system through the capsaicin-sensitive vanilloid receptor (Nakagawa and Hiura, 2006; Silver et al., 2006) and the similarity in chemical structure of the quinones and vanillin moiety, it would seem prudent to test the arthropod-produced quinones on the trigeminal system and specifically on the family of vanilloid receptors. The quinones produced by some bombardier beetles are the result of exothermic reactions that increase the temperature of the secretion to 100 [degrees]C (Eisner, 2003). The high temperature would again stimulate the temperature-sensitive and capsaicin-sensitive vanilloid receptors (Caterina et al., 1997), resulting in a combinatory effect (Dean, 1980). Common phenols and cresols released by millipedes and beetles should also be tested for their activity on known trigeminal receptors.

[FIGURE 3 OMITTED]

Small aliphatic acids are well represented in both data sets, and it is likely that they target the acid-sensitive channel receptor found in the trigeminal system (ASIC) and in sensory neurons involved in taste (Waldman et al., 1997). Acids are also known to modulate the TRPV1 receptors on trigeminal neurons (Tominga et al., 1998; Jordt et al., 2000), and this may play a role in their effectiveness. It has been suggested that the longer-chained aliphatic acids found in arthropod allomone blends serve to improve the penetration of the shorter-chained acids (Eisner et al., 2005). The fact that these compounds in themselves are trigeminal stimulants (Cometto-Muniz et al., 1998) with lower thresholds than the short-chained acids may further enhance their effectiveness.

Our results suggest that a variety of short-chained aldehydes, including trans-2-hexenal and trans-2-octenal, show promise as trigeminal stimulants. The degree of unsaturation and the position of the double bond relative to the aldehyde group are optimal for irritant potential (Alarie et al., 1998). Indeed, while we were preparing this paper, Macpherson et al. (2007) reported that pentenal is a strong agonist of the TRPA1 ion channel. Anisomorphal, the potent lacrimatory agent produced by the two-striped walking stick, Anisomortha buprestoides, also seems likely to have trigeminal activity. Its structure is similar to the very strong trigeminal stimulant acrolein (Nielsen et al., 2007). Aliphatic alcohols are also found in both data sets. Ethanol has been shown to potentiate nociceptive responses in the temperature-sensitive vanilloid receptor (Trevisani et al., 2002).

One might argue that the use of the same chemistries by arthropods belonging to different orders is not convergence but instead a reflection of common ancestry. While this may be true for the chemical pathways leading to the allomonal chemicals themselves, it cannot be true for their use in a defensive context. In most cases, the release mechanism and the glands involved are not homologous. This argues that the use of the same allomones in defense must have evolved repeatedly and truly represents convergence on a common solution to vertebrate predation.

The major arthropod lineages are thought to have had major family-level radiations in the Jurassic period of the Mesozoic (Grimaldi and Engel, 2005). This coincides with the timing of the evolution of small mammals (Pough et al., 2002), which were considered insectivorous (including non-insectan arthropods in their diet as well). Thus the timing is such that small mammals could have been a selective force in the evolution of arthropod defensive chemistry. Chemesthesis is best studied and appears best developed in mammals, but it has homologs in other vertebrate groups (Story and Cruz-Orengo, 2007) and perhaps in non-vertebrates as well.

Perhaps most intriguing are cases in which studies of allomone chemistry reveal a novel suite of compounds that should be tested for trigeminal activity. This is turn may result in the identification of new trigeminal receptors. Polyzonimine, nitropolyzonamine, and buzoamine are novel nitrogen-containing imines and amines released by millipedes of the order Polyzonida (Eisner et al., 2005). The camphor-like odor of these compounds and their ability to repel predators suggest the trigeminal system as a target. One last compound of interest is methyl-anthranilate, a defensive compound released by some ants of the genus Camponotus. Methyl-anthranilate, a natural product also found in the skins of grapes, is a particularly effective trigeminal stimulant and repellent in birds (Kirifides et al., 2004), which are not very sensitive to the mammalian irritant capsaicin (Szolcsanyi, 1993; Jordt and Julius, 2002). In this case, some Camponotus species may produce methyl-anthranilate specifically as an avian repellent. The repellent character of certain compounds thus may not be common to all vertebrates, reflecting differences in their specific trigeminal sensitivities.

Arthropods have provided scientists with an impressive chemical toolbox with which to probe the trigeminal system. Thus far this toolbox has been underutilized. We have here focused on the volatile compounds released by arthropods, but one could easily expand this study to include the waterborne compounds found in venoms and other toxins (e.g., see Siemens et al., 2006). A multidimensional scaling analysis of these compounds could identify additional physiological targets.

Acknowledgments

We thank Dr. Miles Silman for his assistance with the multidimensional scaling ordination. We also acknowledge Dr. Wayne Silver and two anonymous reviewers for their valuable comments on this manuscript.

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WILLIAM E. CONNER*, KERENSA M. ALLEY, JONATHAN R. BARRY, AND AMANDA E. HARPER

Wake Forest University, Department of Biology, Winston-Salem, North Carolina 27106

Received 16 April 2007; accepted 1 August 2007.

* To whom correspondence should be addressed. E-mail: conner@wfu.edu
Table 1 Typical trigeminal stimulants

Volatile stimulants (1)  Water-soluble stimulants

Octanol                  Capsaicin (2)
Nicotine                 Piperine (2)
Heptanol                 Zingerone (2)
Hexanol                  Eugenol (2)
Octanoic acid            Allyl-isothiocyanate (2)
Heptanoic acid           Dihydrocapsaicin (3)
[alpha]-Terpineol        Nordihydrocapsaicin (3)
l-Carvone                Homocapsaicin (3)
Butyric acid             Homodihydrocapsaicin (3)
Pentanol                 Resiniferatoxin (3)
Acetic acid              Isovelleral (3)
Diethylamine             Scutigeral (3)
Cyclohexanone            Capsazepine (3)
Benzaldehyde             Ovanil (3)
Benzyl acetate
Valeric acid
Formic acid
Butanol
Amyl acetate
Ethanol
Propanol
Limonene
Butyl acetate
Toluene
Methanol

(1) Bryant and Silver (2000); in order of increasing threshold.
(2) Alimmohammidi and Silver (2005); in order of decreasing sensitivity.
(3) Nakagawa and Hiura (2006).
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Author:Conner, William E.; Alley, Kerensa M.; Barry, Jonathan R.; Harper, Amanda E.
Publication:The Biological Bulletin
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Date:Dec 1, 2007
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