Chemical Ecology of Cave-Dwelling Millipedes: Defensive Secretions of the Typhloiulini (Diplopoda, Julida, Julidae)

Abstract

Cave animals live under highly constant ecological conditions and in permanent darkness, and many evolutionary adaptations of cave-dwellers have been triggered by their specific environment. A similar “cave effect” leading to pronounced chemical interactions under such conditions may be assumed, but the chemoecology of troglobionts is mostly unknown. We investigated the defensive chemistry of a largely cave-dwelling julid group, the controversial tribe “Typhloiulini”, and we included some cave-dwelling and some endogean representatives. While chemical defense in juliform diplopods is known to be highly uniform, and mainly based on methyl- and methoxy-substituted benzoquinones, the defensive secretions of typhloiulines contained ethyl-benzoquinones and related compounds. Interestingly, ethyl-benzoquinones were found in some, but not all cave-dwelling typhloiulines, and some non-cave dwellers also contained these compounds. On the other hand, ethyl-benzoquinones were not detected in troglobiont nor in endogean typhloiuline outgroups. In order to explain the taxonomic pattern of ethyl-benzoquinone occurrence, and to unravel whether a cave-effect triggered ethyl-benzoquinone evolution, we classed the “Typhloiulini” investigated here within a phylogenetic framework of julid taxa, and traced the evolutionary history of ethyl-benzoquinones in typhloiulines in relation to cave-dwelling. The results indicated a cave-independent evolution of ethyl-substituted benzoquinones, indicating the absence of a “cave effect” on the secretions of troglobiont Typhloiulini. Ethyl-benzoquinones probably evolved early in an epi- or endogean ancestor of a clade including several, but not all Typhloiulus (basically comprising a taxonomic entity known as “Typhloiulus sensu stricto”) and Serboiulus. Ethyl-benzoquinones are proposed as novel and valuable chemical characters for julid systematics.Electronic supplementary materialThe online version of this article (doi:10.1007/s10886-017-0832-1) contains supplementary material, which is available to authorized users.

Millipedes vs. pathogens: Defensive secretions of some julids (Diplopoda: Julida) as potential antimicrobial agents

“…Members of the order Julida, together with spirostreptidans and spirobolidans, are traditionally classified as belonging to the category of “quinone millipedes” [ sensu Eisner, Alsop, Hicks, and Meinwald ()] because the most prominent compounds of their defensive secretion are quinones. Apart from quinones, defensive gland exudates of julidans can contain phenolics, alcohols, aldehydes, esters and anthranilate derivatives (Bodner & Raspotnig, ; Bodner, Vagalinski, Makarov, & Raspotnig, ; Bodner et al., ; Huth, ; Makarov et al., ; Sekulić et al., ; Vujisić et al., ; Wheaterston, Tyrell, & Percy, ; Wheeler, Meinwald, Hurst, & Eisner, ). The typical julidan defensive secretion is a blend of benzoquinones (as dominant compounds) and some of the mentioned compounds, but there are species within this order with an aberrant chemoprofile of defence compounds (Bodner et al., , ; Shimizu, Kuwahara, Yakamuru, & Tanabe, ).…”

Step-wise evolution of complex chemical defenses in millipedes: a phylogenomic approach

“…The production of ethyl-benzoquinones is here only reported for Julidae, Rhinocricidae and Spirostreptidae, which are the three most chemically complex families. Recent analyses for cave-dwelling millipedes, demonstrate that ethyl-benzoquinone production had multiple independent origins, but it is not correlated to cave-dwelling 21 . Our results demonstrate independent origins even at the family level.…”

“…This system ranges from families that produce two chemical molecules (e.g. Nemasomatidae, Parajulidae, Cambalidae, see SI Appendix, Table S1.5 ) to families that can produce over 16 20 , 21 . As new molecule types are discovered and attribute greater chemical complexity to individual millipede families, there is clearly an observed pattern of a positive directional increase within chemical pathways through evolutionary time (Fig.…”

Methyl N-methylanthranilate: major compound in the defensive secretion of Typhloiulus orpheus (Diplopoda, Julida)

“…For 2-ethyl-1,4-benzoquinone we used the defensive secretion of Typhloiulus bureschi and T. georgievi from which this compound had already been identified (Makarov et al 2017). …”

“…Particularly for representatives of the order Julida several aberrant defensive compounds have been described, including phenolics, straight-chain alcohols and aldehydes, and a series of long-chain esters (Wheeler et al 1964 ; Wheaterston et al 1971 ; Huth 2000 ; Vujisic et al 2014 ; Bodner and Raspotnig 2012 ; Shimizu et al 2012 ). Recently, Makarov et al ( 2017 ) investigated the defensive secretions of several species of the so-called “Typhloiulini” (Julida, Julidae) including a recently described endogean species from Bulgaria, Typhloiulus orpheus Vagalinski, Stoev & Enghoff 2015 . The secretion chemistry of T. orpheus was not completely elucidated, but shown to be predominated by one single unusual non-quinonic compound.…”