Versatility of Turing patterns potentiates rapid evolution in tarsal attachment microstructures of stick and leaf insects (Phasmatodea)

Abstract

<jats:p>In its evolution, the diverse group of stick and leaf insects (Phasmatodea) has undergone a rapid radiation. These insects evolved specialized structures to adhere to different surfaces typical for their specific ecological environments. The cuticle of their tarsal attachment pads (euplantulae) is known to possess a high diversity of attachment microstructures (AMS) which are suggested to reflect ecological specializations of different groups within phasmids. However, the origin of these microstructures and their developmental background remain largely unknown. Here, based on the detailed scanning electron microscopy study of pad surfaces, we present a theoretical approach to mathematically model an outstanding diversity of phasmid AMS using the reaction–diffusion model by Alan Turing. In general, this model explains pattern formation in nature. For the first time, we were able to identify eight principal patterns and simulate the transitions among these. In addition, intermediate transitional patterns were predicted by the model. The ease of transformation suggests a high adaptability of the microstructures that might explain the rapid evolution of pad characters. We additionally discuss the functional morphology of the different microstructures and their assumed advantages in the context of the ecological background of species.</jats:p>

Reconstructing the nonadaptive radiation of an ancient lineage of ground‐dwelling stick insects (Phasmatodea: Heteropterygidae)

“…Yet, the Heteropterygidae vary significantly in body size, with Dataminae being comparatively small phasmatodeans whereas Heteropteryginae can be impressively large. The tarsal attachment microstructures have been suggested to be partly associated with body size in Heteropterygidae, although the nonuniformity of this trait may be indicative of the occupation of different niches (Büscher et al ., 2018a, 2018b, 2019) as they reflect adaptations towards different substrate conditions (Büscher & Gorb, 2019; Büscher et al ., 2020). Nevertheless, no notable niche differentiation appears to have occurred in Heteropterygidae, the only exception being Heteropteryx whose green, leaf‐imitating females and flighted males adapted to a secondary tree‐dwelling life style (Bradler & Buckley, 2018).…”

Adhesion Performance in the Eggs of the Philippine Leaf Insect Phyllium philippinicum (Phasmatodea: Phylliidae)

“…Beyond visual aspects, ranging from the imitation of twigs, bark, moss and other environmental elements, along with the convergent evolution of leaf mimicry in Phyliidae and several other groups of stick insects [ 16 ], other characteristics diversified as well. The attachment systems of phasmids, for example, adapted to the abundance of different plant surfaces [ 5 , 17 , 18 , 19 , 20 , 21 ]. Females also made use of a remarkably broad range of oviposition techniques, which differ between species depending on their ecological niche [ 2 , 5 ].…”

Multifunctional Adhesives on the Eggs of the Leaf Insect Phyllium philippinicum (Phasmatodea: Phylliidae): Solvent Influence and Biomimetic Implications

“…Phasmids—also called stick and leaf insects—render proof for a highly connected co-evolution between these herbivore insects and plants. Different aspects of their morphology and physiology, e.g., cryptic masquerade [ 1 , 2 ], oviposition [ 2 , 3 , 4 , 5 , 6 ], as well as their elaborate tarsal attachment systems [ 7 , 8 , 9 , 10 ], substantiate this assertion. Very well-known examples for this aspect of phasmatodean evolution are the Walking Leaves (Phyllidae).…”