Chemosystematics in the Opiliones (Arachnida): a Comment on the Evolutionary History of Alkylphenols and Benzoquinones in the Scent Gland Secretions of Laniatores
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Cladistics Cladistics (2014) 1–8 10.1111/cla.12079 Chemosystematics in the Opiliones (Arachnida): a comment on the evolutionary history of alkylphenols and benzoquinones in the scent gland secretions of Laniatores Gunther€ Raspotniga,b,*, Michaela Bodnera, Sylvia Schaffer€ a, Stephan Koblmuller€ a, Axel Schonhofer€ c and Ivo Karamand aInstitute of Zoology, Karl-Franzens-University, Universitatsplatz€ 2, 8010, Graz, Austria; bResearch Unit of Osteology and Analytical Mass Spectrometry, Medical University, University Children’s Hospital, Auenbruggerplatz 30, 8036, Graz, Austria; cInstitute of Zoology, Johannes Gutenberg University, Johannes-von-Muller-Weg€ 6, 55128, Mainz, Germany; dDepartment of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg Dositeja Obradovica 2, 2100, Novi Sad, Serbia Accepted 2 April 2014 Abstract Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opiliones. These glands pro- duce a variety of chemicals very specific to opilionid taxa of different taxonomic levels, and thus represent a model system to investigate the evolutionary traits in exocrine secretion chemistry across a phylogenetically old group of animals. The chemically best-studied opilionid group is certainly Laniatores, and currently available chemical data allow first hypotheses linking the phy- logeny of this group to the evolution of major chemical classes of secretion chemistry. Such hypotheses are essential to decide upon a best-fitting explanation of the distribution of scent-gland secretion compounds across extant laniatorean taxa, and hence represent a key toward a well-founded opilionid chemosystematics. © The Willi Hennig Society 2014. Introduction Opilionid scent-gland chemistry A recently published chemosystematic approach by Chemical characters from exocrine secretions of Caetano and Machado (2013) to explain the homologous glands offer the opportunity of chemosys- taxonomic distribution of chemical classes of secre- tematic studies based on the principles of cladistics, tion compounds in the large laniatorean family hence introducing an independent set of characters for Gonyleptidae considers benzoquinones ancestral in phylogeny reconstruction in addition to traditional sets this family, vinyl-ketones synapomorphic for one of morphological and molecular data. So far, only a gonyleptid subgroup and alkylphenols as derived few studies have focused on secretion-based chemo- from benzoquinones, having evolved several times systematics along with chemical character evolution in independently. Here, we provide an alternative view the Arthropoda, and only a few arthropod taxa pro- arising from a more adequate ancestral character- vide a promising basis for successful chemosystematic state reconstruction method for secretion chemistry, studies at all. For instance, basic chemosystematic and we furnish evidence for a common ancestry of studies have been conducted for insect groups rich in alkylphenols and the derived status of benzoquinones exocrine glands such as beetles (e.g. Dettner, 1987), in grassatorean secretions. termites (e.g. Prestwich, 1983) and diverse hymenopter- ans (e.g. Cane, 1983), as well as arachnids such as Corresponding author: glandulate oribatid mites (Sakata and Norton, 2001; E-mail address: [email protected] Heethoff et al., 2011; Raspotnig et al., 2011a) and © 2014 The Authors Cladistics published by John Wiley & Sons Ltd on behalf of Willi Hennig Society This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. 2 G. Raspotnig et al. / Cladistics (2014) 1–8 millipedes (e.g. Bodner and Raspotnig, 2012). How- alkylphenols from the ancestral state of benzoquinones ever, another group particularly well suited for chemo- and cited this particular situation as given (Rocha systematics is certainly the Opiliones, the third largest et al., 2013a,b; Wouters et al., 2013). We consider this order of arachnids, comprising about 6500 described proposed evolutionary scenario as rather problematic, species. and show that a few (in our opinion necessary) All opilionids possess large prosomal scent glands, changes in the original data set of Caetano and and the chemistry of scent-gland secretions is stun- Machado as well as in the evaluation method lead to ningly diverse in extant taxa. As opilionids are an completely different results. ancient group of arachnids with fossils known from the Lower Devonian (Dunlop et al., 2004), scent glands represent a well-suited model for studying the Alternative approaches to explain the evolution of evolution of exocrine secretion chemistry in a homolo- laniatorean secretion chemistry gous gland system across hundreds of millions of years. So far, the secretion chemistry in all four We propose to use a more representative selection of opilionid suborders has been exemplarily investigated, gonyleptid outgroups, including also those from which revealing sets of naphthoquinones and methyl ketones alkylphenols have already been reported (“outgroup in the Cyphophthalmi (Raspotnig et al., 2005, 2012), rooting”): in our opinion, outgroup-taxa selection by naphthoquinones in phalangiid Eupnoi (Wiemer et al., Caetano and Machado (2013) was extremely biased, 1978) and in Dyspnoi (Raspotnig et al., 2010), various choosing the only hitherto known non-alkylphenol acycles, including ethyl ketones in sclerosomatid producing manaosbiid as an outgroup. In fact, all Eupnoi (Ekpa et al., 1985), and volatile ketones in chemically investigated grassatorean species outside several Dyspnoi (Raspotnig et al., 2014). The the Gonyleptoidea as well as most basal gonyleptoids chemically best-studied group, however, is certainly exclusively and characteristically produce alkylphenols, the Laniatores, from which at least four major chemi- as outlined below. cal classes of secretion components have been Ancestral character-state reconstruction (ASR) is a reported: (1) nitrogen-containing compounds including frequently used method to test hypotheses regarding various tobacco alkaloids from travunioid Insidiatores character evolution, mainly by mapping characters on (Raspotnig et al., 2011b), and an array of (2) alkyl- given phylogenies, with approaches relying on maxi- phenols, (3) benzoquinones and (4) vinyl-ketones from mum parsimony methods still being most common. As the Grassatores (Roach et al., 1980; Duffield et al., ASR by means of parsimony appears to suffer from 1981; Eisner et al., 2004; Hara et al., 2005; Wouters several limitations (Cunningham, 1999; Ekman et al., et al., 2013). Several authors have hypothesized 2008; Skinner, 2010), many authors have emphasized about the evolutionary history of these compounds, the importance of adapting ASR methods to specific including Hara et al. (2005), Raspotnig et al. (2011b), demands as well as the advantages of comparing Raspotnig (2012) and, recently, Caetano and Machado different ASR approaches for obtaining more differen- (2013). tiated pictures about the evolutionary traits under consideration (e.g. Royer-Carenzi et al., 2013). For instance, the inclusion of likelihood methods may add Evolutionary history of laniatorean secretion chemistry: alternative views of character evolution (e.g. Pagel, current opinions 1999), but requires branch-length information for reli- able ASR and is thus not applicable to analyses that In their recent paper, Caetano and Machado (2013) rely on cladograms. Regarding maximum parsimony- reconstructed the phylogeny of the large laniatorean based ASR, the default approach is often the assign- family Gonyleptidae by combining ecological, behavio- ment of equal costs to character state changes. In ural and chemical characters of 28 species, prior to many cases, however, such an assumption does not mapping the main classes of scent-gland-derived reflect the real situation. How to deal with asymmetric compounds—benzoquinones, alkylphenols and vinyl transformation probabilities, that is, non-equal ketones—onto their phylogenetic tree, by means of probabilities of gains and losses in binary characters, ancestral character-state reconstruction (ASR) under a has been addressed in many studies and may be met parsimony regime of unordered, equal weighted char- by introducing step matrices, making certain transfor- acters. Their results implied benzoquinones to be the mations less likely than others (e.g. Cunningham et al., ancestral state in gonyleptid secretions, vinyl ketones 1998; Ree and Donoghue, 1998; Cunningham, 1999; to be a synapomorphy of gonyleptids of clade “K92,” Omland, 1999). Especially when dealing with chemical and alkylphenols to have evolved five times indepen- compounds in exocrine secretions, it is clear that the dently in the Gonyleptidae. Several authors have acted gain of a compound (its biosynthesis) is much more on the proposal of a multiple independent evolution of difficult, and thus more unlikely, than its loss. The G. Raspotnig et al. / Cladistics (2014) 1–8 3 particular situation of chemosystematics and ASR has Alkylphenols in the Gonyleptoidea been emphasized by, for example, Barkman (2001). In brief, the evolution of a chemical compound requires Chemical data are available for a few representatives an elaborate biosynthetic machinery, which typically of four (of the seven) gonyleptoid families, namely comprises a cascade