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

Abstract

Stick and leaf insects (Phasmatodea) are large terrestrial herbivorous arthropods known for masquerading as plant parts such as bark, twigs and leaves. Their evolutionary history is largely shaped by convergent evolution associated with adaptive radiations on geographically isolated landmasses that have repeatedly generated ground‐dwelling ecomorphs. The members of one lineage, however, the Oriental Heteropterygidae, are morphologically rather uniform, and have a predominantly ground‐dwelling lifestyle. The phylogeny of Heteropterygidae that comprises approximately 130 described species is controversial and remains uncertain. In particular, the systematic position of the giant Jungle Nymph Heteropteryx dilatata, whose males are capable of flight and exhibit the most plesiomorphic wing morphology among extant phasmatodeans, is of major interest to the scientific community. Here, we analysed a set of seven nuclear and mitochondrial genes to infer the phylogeny of Heteropterygidae covering the group's overall diversity. The divergence time estimation and reconstruction of the historical biogeography resulted in an ancestral distribution across Sundaland with long distance dispersal events to Wallacea, the Philippines and the South Pacific. We were able to resolve the relationships among the three principal subgroups of Heteropterygidae and revealed the Dataminae, which contain entirely wingless small forms, as the sister group of Heteropteryginae + Obriminae. Within Heteropteryginae, Haaniella is recovered as paraphyletic in regard to Heteropteryx. Consequently, Heteropteryx must be considered a subordinate taxon deeply embedded within a flightless clade of stick insects. Within Obriminae, the Bornean Hoploclonia is strongly supported as the earliest diverging lineage. Based on this finding, we recognize only two tribes of equal rank among Obriminae, the Hoplocloniini trib. nov. and Obrimini sensu nov. Within the latter, we demonstrate that previous tribal assignments do not reflect phylogenetic relationships and that a basal splitting event occurred between the wing‐bearing clade Miroceramia + Pterobrimus and the remaining wingless Obrimini. The Philippine genus Tisamenus is paraphyletic with regard to Ilocano hebardi, thus, we transfer the latter species to Tisamenus as Tisamenus hebardi comb. nov. and synonymize Ilocano with Tisamenus. We discuss character transformations in the light of the new phylogenetic results and conclude that the current taxonomic diversity appears to be mainly driven by allopatry and not to be the result of niche differentiation. This radiation is thus best described as a nonadaptive radiation.

A tree of leaves: Phylogeny and historical biogeography of the leaf insects (Phasmatodea: Phylliidae)

“…1 – 5 ). The outgroup taxa adapted from Bank et al 26 were found to present a similar topology with minor differences in regard to weakly supported sister group relationships (Supplementary Fig. 1 ).…”

“…Adapted to a tree-dwelling life style, phylliid masquerade is achieved by simulating the broad leaves of flowering plants and the additional imitation of the diffuse growth of leaf veins in the female forewing venation 19 that has perfected their cryptic appearance in the foliage. This uniform adaptation is best described as a nonadaptive radiation in which the diversification was not accompanied by relevant niche differentiation 50 , resulting in taxa with little or no ecological and phenotypic variation 51 , as has been recently suggested for a clade of uniformly ground-dwelling stick insects 26 . Both the broad leaf habitus and the net venation of Phylliidae are evidently linked to the eudicot angiosperm evolution.…”

“…Phylliidae are recovered in all trees as the sister group to the remaining Neophasmatodea, a topology that was also obtained in some previous studies based on just seven or fewer loci 24 – 26 . This might actually be artificial due to a bias resulting from the similarity of these loci to Aschiphasmatidae, which were recently estimated to be the sister group to Phylliidae 41 .…”

“…From Borneo, several lineages have independently colonised the islands of the Philippines and Wallacea, as well as Western Indonesia and the Malay Peninsula. While the Philippines were most likely colonised from Borneo via the Sulu archipelago 100 , 101 , the colonisation from Wallacea probably occurred across the island arc of the Sangihe-Talaud archipelago 26 , 99 , 100 , 102 . In contrast to the other leaf insect genera, Phyllium colonised multiple islands and regions, resulting in a high number of independent speciation events.…”

Physical constraints lead to parallel evolution of micro- and nanostructures of animal adhesive pads: a review

“…Stick and leaf insects are an impressive model group for the exploration of many evolutionary aspects, especially convergence. Limited spatial dispersion and extensive adaptive radiation led to a high degree of convergent traits in Phasmatodea, (e.g., in terms of visual camouflage [184][185][186][187], oviposition techniques [109,[188][189][190][191][192][193][194], different degrees of wing loss [195][196][197], and ecomorphs (morphological forms with similar ecological occupancy) with specific vertical stratification within the vegetation [108,198,199]). Phasmids are predominantly nocturnal insects that are distributed nearly worldwide and exceptionally herbivorous [184][185][186][187]194,200], with the highest diversity in the tropics.…”