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

ABSTRACT: The insect order Phasmatodea is known for large slender insects masquerading as twigs or bark. In contrast to these so-called stick insects, the subordinated clade of leaf insects (Phylliidae) are dorso-ventrally flattened and therefore resemble leaves in a unique way. Here we show that the origin of extant leaf insects lies in the Australasian/Pacific region with subsequent dispersal westwards to mainland Asia and colonisation of most Southeast Asian landmasses. We further hypothesise that the clade originated in the Early Eocene after the emergence of angiosperm-dominated rainforests. The genus Phyllium to which most of the ~100 described species pertain is recovered as paraphyletic and its three non-nominate subgenera are recovered as distinct, monophyletic groups and are consequently elevated to genus rank. This first phylogeny covering all major phylliid groups provides the basis for future studies on their taxonomy and a framework to unveil more of their cryptic and underestimated diversity.

SUBMITTER: Bank S

PROVIDER: S-EPMC8329230 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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

Bank Sarah S Cumming Royce T RT Li Yunchang Y Henze Katharina K Le Tirant Stéphane S Bradler Sven S

Communications biology 20210802 1

The insect order Phasmatodea is known for large slender insects masquerading as twigs or bark. In contrast to these so-called stick insects, the subordinated clade of leaf insects (Phylliidae) are dorso-ventrally flattened and therefore resemble leaves in a unique way. Here we show that the origin of extant leaf insects lies in the Australasian/Pacific region with subsequent dispersal westwards to mainland Asia and colonisation of most Southeast Asian landmasses. We further hypothesise that the ...[more]

PMID: 34341467

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Project description:While the leaf insects (Phylliidae) are a well-supported group within Phasmatodea, the genus Phyllium Illiger, 1798 has repeatedly been recovered as paraphyletic. Here, the Phyllium (Phyllium) celebicum species group is reviewed and its distinctiveness from the remaining Phylliini genera and subgenera in a phylogenetic context based on morphological review and a phylogenetic analysis of three genes (nuclear gene 28S and mitochondrial genes COI and 16S) from most known and multiple undescribed species is shown. A new genus, Cryptophyllium gen. nov., is erected to partially accommodate the former members of the celebicum species group. Two species, Phyllium ericoriaiHennemann et al., 2009 and Phyllium bonifacioi Lit & Eusebio, 2014 morphologically and molecularly do not fall within this clade and are therefore left within Phyllium (Phyllium). The transfer of the remaining celebicum group members from Phyllium Illiger, 1798 to this new genus creates the following new combinations; Cryptophyllium athanysus (Westwood, 1859), comb. nov.; Cryptophyllium celebicum (de Haan, 1842), comb. nov.; Cryptophyllium chrisangi (Seow-Choen, 2017), comb. nov.; Cryptophyllium drunganum (Yang, 1995), comb. nov.; Cryptophyllium oyae (Cumming & Le Tirant, 2020), comb. nov.; Cryptophyllium parum (Liu, 1993), comb. nov.; Cryptophyllium rarum (Liu, 1993), comb. nov.; Cryptophyllium tibetense (Liu, 1993), comb. nov.; Cryptophyllium westwoodii (Wood-Mason, 1875), comb. nov.; Cryptophyllium yapicum (Cumming & Teemsma, 2018), comb. nov.; and Cryptophyllium yunnanense (Liu, 1993), comb. nov. The review of specimens belonging to this clade also revealed 13 undescribed species, which are described within as: Cryptophyllium animatum gen. et sp. nov. from Vietnam: Quang Nam Province; Cryptophyllium bankoi gen. et sp. nov. from Vietnam: Quang Ngai, Thua Thien Hue, Da Nang, Gia Lai, Quang Nam, and Dak Nong Provinces; Cryptophyllium bollensi gen. et sp. nov. from Vietnam: Ninh Thuan Province; Cryptophyllium daparo gen. et sp. nov. from China: Yunnan Province; Cryptophyllium echidna gen. et sp. nov. from Indonesia: Wangi-wangi Island; Cryptophyllium faulkneri gen. et sp. nov. from Vietnam: Quang Ngai and Lam Dong Provinces; Cryptophyllium icarus gen. et sp. nov. from Vietnam: Lam Dong and Dak Lak Provinces; Cryptophyllium khmer gen. et sp. nov. from Cambodia: Koh Kong and Siem Reap Provinces; Cryptophyllium limogesi gen. et sp. nov. from Vietnam: Lam Dong, Dak Lak, and Dak Nong Provinces; Cryptophyllium liyananae gen. et sp. nov. from China: Guangxi Province; Cryptophyllium nuichuaense gen. et sp. nov. from Vietnam: Ninh Thuan Province; Cryptophyllium phami gen. et sp. nov. from Vietnam: Dong Nai and Ninh Thuan Provinces; and Cryptophyllium wennae gen. et sp. nov. from China: Yunnan Province. All newly described species are morphologically described, illustrated, and molecularly compared to congenerics. With the molecular results revealing cryptic taxa, it was found necessary for Cryptophyllium westwoodii (Wood-Mason, 1875), comb. nov. to have a neotype specimen designated to allow accurate differentiation from congenerics. To conclude, male and female dichotomous keys to species for the Cryptophyllium gen. nov. are presented.

Project description:Phylliidae are herbivorous insects exhibiting impressive cryptic masquerade and are colloquially called "walking leaves". They imitate angiosperm leaves and their eggs often resemble plant seeds structurally and in some cases functionally. Despite overall morphological similarity of adult Phylliidae, their eggs reveal a significant diversity in overall shape and exochorionic surface features. Previous studies have shown that the eggs of most Phylliidae possess a specialised attachment mechanism with hierarchical exochorionic fan-like structures (pinnae), which are mantled by a film of an adhesive secretion (glue). The folded pinnae and glue respond to water contact, with the fibrous pinnae expanding and the glue being capable of reversible liquefaction. In general, the eggs of phylliids appear to exhibit varying structures that were suggested to represent specific adaptations to the different environments the eggs are deposited in. Here, we investigated the diversity of phylliid eggs and the functional morphology of their exochorionic structure. Based on the examination of all phylliid taxa for which the eggs are known, we were able to characterise eleven different morphological types. We explored the adhesiveness of these different egg morphotypes and experimentally compared the attachment performance on a broad range of substrates with different surface roughness, surface chemistry and tested whether the adhesion is replicable after detachment in multiple cycles. Furthermore, we used molecular phylogenetic methods to reconstruct the evolutionary history of different egg types and their adhesive systems within this lineage, based on 53 phylliid taxa. Our results suggest that the egg morphology is congruent with the phylogenetic relationships within Phylliidae. The morphological differences are likely caused by adaptations to the specific environmental requirements for the particular clades, as the egg morphology has an influence on the performance regarding the surface roughness. Furthermore, we show that different pinnae and the adhesive glue evolved convergently in different species. While the evolution of the Phylliidae in general appears to be non-adaptive judging on the strong similarity of the adults and nymphs of most species, the eggs represent a stage with complex and rather diverse functional adaptations including mechanisms for both fixation and dispersal of the eggs.

Project description:With the first large-scale Phylliidae molecular phylogeny recently published adding a great deal of clarity to phylliid diversity, several of the rarer species which could not be included were methodically and morphologically reviewed. This review resulted in identification of numerous substantial morphological features that suggest there are Melanesian clades that create polyphyletic groups within the phylliids which should instead be taxonomically recognized as unique. These rarer Melanesia species have historically been considered to be southern representatives of the Pulchriphyllium Griffini, 1898 sensu lato. However, there are notable morphological differences between the Pulchriphyllium sensu stricto and the "schultzei" group. Therefore, two new genera are erected, Vaabonbonphyllium gen. nov. from the Solomon Islands and Papua New Guinea and Rakaphyllium gen. nov. from New Guinea and the Aru Islands. Erection of these two new genera warrants the following new combinations: Rakaphylliumschultzei (Giglio-Tos, 1912), comb. nov., Rakaphylliumexsectum (Zompro, 2001b), comb. nov., and Vaabonbonphylliumgroesseri (Zompro, 1998), comb. nov. Additionally, while reviewing material an undescribed Vaabonbonphyllium gen. nov. specimen was located and is herein described as Vaabonbonphylliumrafidahae gen. et sp. nov. from Mt. Hagen, Papua New Guinea. Additionally, a morphologically unique clade of several species recovered as sister to the Nanophyllium sensu stricto was recognized and their numerous unique morphological features and monophyly leads the authors to erect the new genus Acentetaphyllium gen. nov. which warrants the following new combinations: Acentetaphylliumbrevipenne (Größer, 1992), comb. nov., Acentetaphylliumlarssoni (Cumming, 2017), comb. nov., Acentetaphylliummiyashitai (Cumming et al. 2020), comb. nov., and Acentetaphylliumstellae (Cumming, 2016), comb. nov. With the addition of several new genera, a key to phylliid genera is included for adult males and females.

Dataset Information

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

Publications

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

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