Variation and specialisation of the forcipular apparatus of centipedes (Arthropoda: Chilopoda): a comparative morphometric and microscopic investigation of an evolutionary novelty.

The forcipules of centipedes are the only known example in the animal kingdom of an evolutionary transition from walking legs to venom-injecting appendages. They provide a classic case of an evolutionary novelty under most (but not all) definitions of that concept. Although there is a reasonable literature on forcipules, and on the forcipular segment more generally, it is fragmentary and scattered. Also, many previous studies have been based on a single species and hence have no comparative component. Here, we build on this earlier literature by providing detailed qualitative and quantitative information on the forcipular segments of representatives of the five extant orders of centipedes. Our results reveal notable differences between the orders - as well as considerable variation within some of them. The pattern of inter-group differences can be used to infer, albeit cautiously, a major evolutionary trend from a presumed scutigeromorph-like last common ancestor (LCA), in which the forcipules were probably leg-like (as in present-day scutigeromorphs) to a more specialized claw-like structure with movement restricted to the horizontal plane. This morphological trend may reflect an ecological trend from open-habitat ambush predation to leaf-litter and subterranean predatory opportunism.

Dugon MM ，Black A ，Arthur W 《-》

Comparative studies on the structure and development of the venom-delivery system of centipedes, and a hypothesis on the origin of this evolutionary novelty.

The venom-injecting forcipules of centipedes represent an evolutionary novelty that appeared in the centipede stem lineage more than 400 Ma. No other lineage of arthropods (or indeed of animals) has evolved claws for injecting venom from a pair of walking legs. However, little is known of the development, ultrastructure, or detailed function of centipede forcipules. Here, we provide comparative structural information on the venom duct apparatus that is the main functional system within each forcipule, based on scanning electron microscopy and transmission electron microscopy studies. We also give comparative developmental information, using DAPI staining, on embryonic forcipules from the four main centipede orders, including Scutigeromorpha. The photographs of Scutigera embryos we present are the first to be published for any species belonging to this order. The structure of the venom apparatus within each forcipule represents a discrete element of the novelty, whose origin requires a special explanation. This is in contrast to the novel external shape of the forcipules, which can be arrived at gradually by a series of changes from the starting point of a standard walking leg. Drawing on a proposed structural homology between venom glands and epidermal glands, we present a hypothesis of how the venom gland and duct may have arisen in evolution.

Dugon MM ，Arthur W 《-》

Presence of morphological integration and modularity of the forcipular apparatus in Lithobius melanops (Chilopoda: Lithobiomorpha: Lithobiidae).

The presence of morphological integration and modularity of the forcipular apparatus, despite its evolutionary significance, has not been analyzed in centipedes. This morphological structure has a crucial role in feeding and defense, thanks to its poisonous part (forcipules), which is important for catching the prey. The aims of our study were: i) to test the hypothesis of modularity of the forcipular apparatus in centipede Lithobius melanops; and ii) to investigate the influence of allometry on overall morphological integration in the aforementioned species using a geometric morphometric approach. The presence of fluctuating asymmetry was obtained by Procrustes ANOVA. Allometry was significant only for the symmetric component of the forcipular apparatus. The modularity hypothesis was not accepted, because the covariance coefficients for symmetric and asymmetric components were lower than 89.5% and 72.1% (respectively) of other RV coefficients obtained by a random contiguous partition of the forcipular apparatus. Results of the present study indicate that allometry does increase the level of morphological integration in the forcipular apparatus. According to our results, the forcipular coxosternite and forcipules could not be considered as separate modules; namely, they probably share similar developmental pathways and function in different forms of behavior and survival in L. melanops.

Vujić VD ，Ilić BS ，Lučić LR ，Jovanović ZS ，Milovanović JZ ，Dudić BD ，Stojanović DZ ... -  《-》

Expression patterns of Wnt genes in the venom claws of centipedes.

The venom claws of centipedes, also known as forcipules, represent an evolutionary novelty that must have arisen in the centipede stem species, as they are not found in any other myriapods. The developmental-genetic changes that are involved in the origin of novelties are of considerable interest. It has previously been shown that centipede forcipules have a unique Hox code. However, this is a combinatorial code: no single Hox gene has a forcipule-specific expression. Here, we focus on Wnt genes. Two genes of this family show forcipule-specific expression in the "model centipede" Strigamia maritima: Wnt7 and Wnt11. For Wnt7, this forcipular expression zone seems to be a new one, which has arisen in evolution subsequently to other expression zones of the same gene. However, for Wnt11, the forcipule-specific expression probably arose by reduction of a more general pattern that originally included most or all of the limbs of an ancestral myriapod. Thus the developmental-genetic basis of the evolutionary change that turned the first pair of walking legs into venom claws is complex, involving different types of change in expression pattern. This sort of complexity is likely to be the case regarding evolutionary changes in morphology in general. Whether the origins of those features that can be considered as novelties are different in terms of their developmental-genetic basis from more routine evolutionary changes remains an open question.

Hayden L ，Arthur W 《-》

Material composition and mechanical properties of the venom-injecting forcipules in centipedes.

Centipedes are terrestrial and predatory arthropods that possess an evolutionary transformed pair of appendages used for venom injection-the forcipules. Many arthropods incorporate reinforcing elements into the cuticle of their piercing or biting structures to enhance hardness, elasticity or resistance to wear and structural failure. Given their frequent exposure to high mechanical stress, we hypothesise that the cuticle of the centipede forcipule might be mechanically reinforced. With a combination of imaging, analytical techniques and mechanical testing, we explore the centipede forcipule in detail to shed light on its morphology and performance. Additionally, we compare these data to characteristics of the locomotory leg to infer evolutionary processes. We examined sclerotization patterns using confocal laser-scanning microscopy based on autofluorescence properties of the cuticle (forcipule and leg) and elemental composition by energy-dispersive X-ray spectroscopy in representative species from all five centipede lineages. These experiments revealed gradually increasing sclerotization towards the forcipular tarsungulum and a stronger sclerotization of joints in taxa with condensed podomeres. Depending on the species, calcium, zinc or chlorine are present with a higher concentration towards the distal tarsungulum. Interestingly, these characteristics are more or less mirrored in the locomotory leg's pretarsal claw in Epimorpha. To understand how incorporated elements affect mechanical properties, we tested resistance to structural failure, hardness (H) and Young's modulus (E) in two representative species, one with high zinc and one with high calcium content. Both species, however, exhibit similar properties and no differences in mechanical stress the forcipule can withstand. Our study reveals similarities in the material composition and properties of the forcipules in centipedes. The forcipules transformed from an elongated leg-like appearance into rigid piercing structures. Our data supports their serial homology to the locomotory leg and that the forcipule's tarsungulum is a fusion of tarsus and pretarsal claw. Calcium or zinc incorporation leads to comparable mechanical properties like in piercing structures of chelicerates and insects, but the elemental incorporation does not increase H and E in centipedes, suggesting that centipedes followed their own pathways in the evolutionary transformation of piercing tools.

Züger S ，Krings W ，Gorb SN ，Büscher TH ，Sombke A ... -  《Frontiers in Zoology》