Limits...
Chemosystematics in the Opiliones (Arachnida): a comment on the evolutionary history of alkylphenols and benzoquinones in the scent gland secretions of Laniatores.

Raspotnig G, Bodner M, Schäffer S, Koblmüller S, Schönhofer A, Karaman I - Cladistics (2014)

Bottom Line: Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opiliones.The chemically best-studied opilionid group is certainly Laniatores, and currently available chemical data allow first hypotheses linking the phylogeny 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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Zoology, Karl-Franzens-University Universitätsplatz 2, 8010, Graz, Austria ; Research Unit of Osteology and Analytical Mass Spectrometry, Medical University, University Children's Hospital Auenbruggerplatz 30, 8036, Graz, Austria.

ABSTRACT

Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opiliones. These glands produce 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 phylogeny 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.

No MeSH data available.


Ancestral character-state reconstruction of the scent-gland associated characters “alkylphenols” and “benzoquinones” with an indication of its interpretion, again using the tree of Fig.1. As indicated by their biosynthesis, benzoquinones are considered derived from the ancestral state of alkylphenols by p-oxidation (Rocha et al., 2013a), thus a maximum parsimony reconstruction, relying on ordered characters, is shown (character state “green”: alkylphenols; character state “black”: benzoquinones). (1) The common biosynthethic pathway to alkylphenols and benzoquinones is ancestral and evolved in basal grassatoreans. Benzoquinones are derived from the ancestral state of alkylphenols, mainly relying on phenol p-oxidation. (2) The extension of the pathway from alkylphenols to benzoquinones may have happened in gonyleptoids after the split-off of the Stygnopsidae. (3) In a number of gonyleptoid taxa, however, this final step to benzoquinone synthesis has been lost independently, again leading to the ancestral state of alkylphenols. (4) In other taxa, both alkylphenols and benzoquinones have been lost completely. Note the travunioid Insidiatores (outgroup) that primarily produce neither alkylphenols nor benzoquinones but rely on nitrogen-compound-rich secretions (Raspotnig et al., 2011b). Note the gonyleptid clade “K92” in which alkylphenol and/or benzoquinones are frequently reduced; the whole clade is characterized by vinyl-ketone-rich secretions (not indicated, see Caetano and Machado, 2013).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4459239&req=5

fig02: Ancestral character-state reconstruction of the scent-gland associated characters “alkylphenols” and “benzoquinones” with an indication of its interpretion, again using the tree of Fig.1. As indicated by their biosynthesis, benzoquinones are considered derived from the ancestral state of alkylphenols by p-oxidation (Rocha et al., 2013a), thus a maximum parsimony reconstruction, relying on ordered characters, is shown (character state “green”: alkylphenols; character state “black”: benzoquinones). (1) The common biosynthethic pathway to alkylphenols and benzoquinones is ancestral and evolved in basal grassatoreans. Benzoquinones are derived from the ancestral state of alkylphenols, mainly relying on phenol p-oxidation. (2) The extension of the pathway from alkylphenols to benzoquinones may have happened in gonyleptoids after the split-off of the Stygnopsidae. (3) In a number of gonyleptoid taxa, however, this final step to benzoquinone synthesis has been lost independently, again leading to the ancestral state of alkylphenols. (4) In other taxa, both alkylphenols and benzoquinones have been lost completely. Note the travunioid Insidiatores (outgroup) that primarily produce neither alkylphenols nor benzoquinones but rely on nitrogen-compound-rich secretions (Raspotnig et al., 2011b). Note the gonyleptid clade “K92” in which alkylphenol and/or benzoquinones are frequently reduced; the whole clade is characterized by vinyl-ketone-rich secretions (not indicated, see Caetano and Machado, 2013).

Mentions: For our ASR approach, we thus used the tree proposed by Caetano and Machado, supplemented by outgroups on which chemical information has previously been published. In particular, we added non-grassatoreans such as travunioids, non-gonyleptoid grassatoreans such as phalangodids, stygnommatids and gonyleptoids such as stygnopsids, as well as manaosbiids and cosmetids (Figs1 and 2). These additional taxa, in particular the lower grassatorean families, were placed as proposed in the laniatorean phylogeny of Sharma and Giribet (2011). For cosmetids, we chose to show a polytomy for all chemically analysed species, because their phylogenetic relationships are still unresolved. All other aspects in the tree of Caetano and Machado were left unchanged. We subsequently performed ACRs under different assumptions: (I) under an unordered parsimony regime of equal-weighted gains and losses (as done by Caetano and Machado, 2013); (II) under a parsimony regime using step matrices, making gains less likely than losses; and (III) under an ordered parsimony regime, accounting for information on the dependency of alkylphenol and benzoquinone production in gonyleptids and the reversible conversion of alkylphenols to benzoquinones (Rocha et al., 2013a). All reconstructions were conducted in Mesquite Version 2.75 (Maddison and Maddison, 2011). The ASR was based on a single-tree input, thus it was not possible to account for topological uncertainty in the analysis. The reconstructions obtained (I–III) show diverging results. In (I) the ASR using the parsimony approach under equal weights for gains and losses still indicates that alkylphenols arose several times independently in the Gonyleptidae even though they are indicated to represent old grassatorean equipment as evidenced from outgroups, basically being consistent with the findings of Caetano and Machado (2013; not shown). As this kind of reconstruction ignores the above-mentioned differences in probabilities of gaining or losing a particular trait as well as information on a common route of alkylphenol and benzoquinone biosynthesis, we believe that this reconstruction does not adequately reflect alkylphenol evolution. By contrast, reconstruction (II), an ASR approach using weighted parsimony, strongly suggests a common alkylphenol ancestry (Fig.1). Considering a multistep biosynthesis of alkylphenols from acetate and propionate units, as recently suggested by Rocha et al. (2013a), a step-matrix making gains several times less likely than losses might be proposed. For Magnispina neptunus (Heteropachylinae), a known benzoquinone producer, the route to its main secretion component 2-ethyl-1,4-benzoquinone might include at least six steps (scheme 1 in Rocha et al., 2013a), starting with the repeated condensation of acetate units to form a polyketide chain, followed by cyclization, enolysation and decarboxylation, then resulting in an ethylphenol. Phenol p-oxidation leads to the corresponding ethyl-1,4-hydroquinone, and further oxidation to the ethyl-1,4-benzoquinone. According to Rocha et al. (2013a), small amounts of the intermediate hydroquinones can generally be detected in benzoquinone-producing Gonyleptidae. An ACR on phenols and benzoquinones must take such a multistep biosynthesis into account. Indeed, even when introducing a rather low weighting factor of three (for gains) into a step matrix, a scenario as pictured in Fig.1 arises, indicating that alkylphenols are ancestral in grassatorean secretions, having evolved only once in early grassatoreans. In (III), using an ordered parsimony approach as strongly implied by alkylphenol and benzoquinone biosynthesis, the scenario of Fig.2 arises, and should be interpreted as follows: a common biosynthetic pathway to alkylphenols and benzoquinones evolved only once. Benzoquinones are derived from ancestral alkylphenols by p-oxidation and benzoquinones replaced alkylphenols in the Gonyleptoidea higher than Stygnopsidae. The final biosynthetic step toward benzoquinones is indicated to have been lost several times independently (seven times when using the approach herein, see Fig.2). Such a scenario requires only the loss of p-oxidation, being much more likely than the multiple independent development of the whole biosynthetic machinery toward alkylphenols. The picture obtained from this ordered parsimony approach superficially resembles the reconstruction from Caetano and Machado (2013), but it shows a completely different pattern of alkylphenol and benzoquinone evolution in gonyleptoid harvestmen.


Chemosystematics in the Opiliones (Arachnida): a comment on the evolutionary history of alkylphenols and benzoquinones in the scent gland secretions of Laniatores.

Raspotnig G, Bodner M, Schäffer S, Koblmüller S, Schönhofer A, Karaman I - Cladistics (2014)

Ancestral character-state reconstruction of the scent-gland associated characters “alkylphenols” and “benzoquinones” with an indication of its interpretion, again using the tree of Fig.1. As indicated by their biosynthesis, benzoquinones are considered derived from the ancestral state of alkylphenols by p-oxidation (Rocha et al., 2013a), thus a maximum parsimony reconstruction, relying on ordered characters, is shown (character state “green”: alkylphenols; character state “black”: benzoquinones). (1) The common biosynthethic pathway to alkylphenols and benzoquinones is ancestral and evolved in basal grassatoreans. Benzoquinones are derived from the ancestral state of alkylphenols, mainly relying on phenol p-oxidation. (2) The extension of the pathway from alkylphenols to benzoquinones may have happened in gonyleptoids after the split-off of the Stygnopsidae. (3) In a number of gonyleptoid taxa, however, this final step to benzoquinone synthesis has been lost independently, again leading to the ancestral state of alkylphenols. (4) In other taxa, both alkylphenols and benzoquinones have been lost completely. Note the travunioid Insidiatores (outgroup) that primarily produce neither alkylphenols nor benzoquinones but rely on nitrogen-compound-rich secretions (Raspotnig et al., 2011b). Note the gonyleptid clade “K92” in which alkylphenol and/or benzoquinones are frequently reduced; the whole clade is characterized by vinyl-ketone-rich secretions (not indicated, see Caetano and Machado, 2013).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4459239&req=5

fig02: Ancestral character-state reconstruction of the scent-gland associated characters “alkylphenols” and “benzoquinones” with an indication of its interpretion, again using the tree of Fig.1. As indicated by their biosynthesis, benzoquinones are considered derived from the ancestral state of alkylphenols by p-oxidation (Rocha et al., 2013a), thus a maximum parsimony reconstruction, relying on ordered characters, is shown (character state “green”: alkylphenols; character state “black”: benzoquinones). (1) The common biosynthethic pathway to alkylphenols and benzoquinones is ancestral and evolved in basal grassatoreans. Benzoquinones are derived from the ancestral state of alkylphenols, mainly relying on phenol p-oxidation. (2) The extension of the pathway from alkylphenols to benzoquinones may have happened in gonyleptoids after the split-off of the Stygnopsidae. (3) In a number of gonyleptoid taxa, however, this final step to benzoquinone synthesis has been lost independently, again leading to the ancestral state of alkylphenols. (4) In other taxa, both alkylphenols and benzoquinones have been lost completely. Note the travunioid Insidiatores (outgroup) that primarily produce neither alkylphenols nor benzoquinones but rely on nitrogen-compound-rich secretions (Raspotnig et al., 2011b). Note the gonyleptid clade “K92” in which alkylphenol and/or benzoquinones are frequently reduced; the whole clade is characterized by vinyl-ketone-rich secretions (not indicated, see Caetano and Machado, 2013).
Mentions: For our ASR approach, we thus used the tree proposed by Caetano and Machado, supplemented by outgroups on which chemical information has previously been published. In particular, we added non-grassatoreans such as travunioids, non-gonyleptoid grassatoreans such as phalangodids, stygnommatids and gonyleptoids such as stygnopsids, as well as manaosbiids and cosmetids (Figs1 and 2). These additional taxa, in particular the lower grassatorean families, were placed as proposed in the laniatorean phylogeny of Sharma and Giribet (2011). For cosmetids, we chose to show a polytomy for all chemically analysed species, because their phylogenetic relationships are still unresolved. All other aspects in the tree of Caetano and Machado were left unchanged. We subsequently performed ACRs under different assumptions: (I) under an unordered parsimony regime of equal-weighted gains and losses (as done by Caetano and Machado, 2013); (II) under a parsimony regime using step matrices, making gains less likely than losses; and (III) under an ordered parsimony regime, accounting for information on the dependency of alkylphenol and benzoquinone production in gonyleptids and the reversible conversion of alkylphenols to benzoquinones (Rocha et al., 2013a). All reconstructions were conducted in Mesquite Version 2.75 (Maddison and Maddison, 2011). The ASR was based on a single-tree input, thus it was not possible to account for topological uncertainty in the analysis. The reconstructions obtained (I–III) show diverging results. In (I) the ASR using the parsimony approach under equal weights for gains and losses still indicates that alkylphenols arose several times independently in the Gonyleptidae even though they are indicated to represent old grassatorean equipment as evidenced from outgroups, basically being consistent with the findings of Caetano and Machado (2013; not shown). As this kind of reconstruction ignores the above-mentioned differences in probabilities of gaining or losing a particular trait as well as information on a common route of alkylphenol and benzoquinone biosynthesis, we believe that this reconstruction does not adequately reflect alkylphenol evolution. By contrast, reconstruction (II), an ASR approach using weighted parsimony, strongly suggests a common alkylphenol ancestry (Fig.1). Considering a multistep biosynthesis of alkylphenols from acetate and propionate units, as recently suggested by Rocha et al. (2013a), a step-matrix making gains several times less likely than losses might be proposed. For Magnispina neptunus (Heteropachylinae), a known benzoquinone producer, the route to its main secretion component 2-ethyl-1,4-benzoquinone might include at least six steps (scheme 1 in Rocha et al., 2013a), starting with the repeated condensation of acetate units to form a polyketide chain, followed by cyclization, enolysation and decarboxylation, then resulting in an ethylphenol. Phenol p-oxidation leads to the corresponding ethyl-1,4-hydroquinone, and further oxidation to the ethyl-1,4-benzoquinone. According to Rocha et al. (2013a), small amounts of the intermediate hydroquinones can generally be detected in benzoquinone-producing Gonyleptidae. An ACR on phenols and benzoquinones must take such a multistep biosynthesis into account. Indeed, even when introducing a rather low weighting factor of three (for gains) into a step matrix, a scenario as pictured in Fig.1 arises, indicating that alkylphenols are ancestral in grassatorean secretions, having evolved only once in early grassatoreans. In (III), using an ordered parsimony approach as strongly implied by alkylphenol and benzoquinone biosynthesis, the scenario of Fig.2 arises, and should be interpreted as follows: a common biosynthetic pathway to alkylphenols and benzoquinones evolved only once. Benzoquinones are derived from ancestral alkylphenols by p-oxidation and benzoquinones replaced alkylphenols in the Gonyleptoidea higher than Stygnopsidae. The final biosynthetic step toward benzoquinones is indicated to have been lost several times independently (seven times when using the approach herein, see Fig.2). Such a scenario requires only the loss of p-oxidation, being much more likely than the multiple independent development of the whole biosynthetic machinery toward alkylphenols. The picture obtained from this ordered parsimony approach superficially resembles the reconstruction from Caetano and Machado (2013), but it shows a completely different pattern of alkylphenol and benzoquinone evolution in gonyleptoid harvestmen.

Bottom Line: Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opiliones.The chemically best-studied opilionid group is certainly Laniatores, and currently available chemical data allow first hypotheses linking the phylogeny 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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Zoology, Karl-Franzens-University Universitätsplatz 2, 8010, Graz, Austria ; Research Unit of Osteology and Analytical Mass Spectrometry, Medical University, University Children's Hospital Auenbruggerplatz 30, 8036, Graz, Austria.

ABSTRACT

Large prosomal scent glands constitute a major synapomorphic character of the arachnid order Opiliones. These glands produce 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 phylogeny 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.

No MeSH data available.