The phasmatodean tree of life: resolving evolutionary patterns of diversity and disparity in a mesodiverse insect lineage

• Applicant: Privatdozent Dr. Sven Bradler
• Subject Area: Systematics and Morphology (Zoology)
• Term: from 2017 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 337291343

• Final Report Year: 2024

Final Report Abstract

Stick and leaf insects, or Phasmatodea, are a mesodiverse lineage of large terrestrial herbivorous arthropods with predominantly tropical and subtropical distribution. They are usually nocturnal and exhibit remarkable forms of masquerade crypsis, imitating various parts of plants, such as twigs, bark and leaves to deceive visually hunting predators. Phasmatodea comprises ~3500 extant described species and serves as a model system to address relevant questions in evolutionary biology. Until recently, stick and leaf insects stood out as one of the last remaining insect orders without a robust higher-level phylogenetic hypothesis. Our molecular analyses based on transcriptomic and Sanger sequence data have now largely resolved the evolutionary relationships of these insects and corroborate the finding that the extant diversity is the result of a surprisingly recent rapid radiation. Our temporally calibrated phylogenetic analysis is based on data selected for maximum phylogenetic coverage from over 1000 stick and leaf insect species. For some crucial taxa and evolutionary lineages we nevertheless obtained conflicting phylogenetic hypotheses due to lack of sufficient data. We further expanded our studies and applied target enrichment to reliably reconstruct the relationships of these problematic taxa. We recovered a previously unrecognized major New World and Old World lineage, for which we introduced the new names Oriophasmata (“Eastern phasmids”) and Occidophasmata (“Western phasmids”), containing the bulk of extant stick and leaf insects. The obtained tree provided the evolutionary framework for (i) tracing the global historical biogeography of phasmatodeans, (ii) assessing rates of speciation and extinction, (iii) reconstructing ancestral character states and transformations of crucial traits that are involved in adaptive radiations, and (iv) detecting numerous undescribed species, which resulted in the formal description of more than two dozen new taxa. Our analyses furthermore revealed a high degree of convergent evolution in regard of reproductive strategies, tarsal attachment structures and various ecomorphs. The previously assumed and highly debated scenario of an ancestral loss of wings in stick insects with repeated wing regain in subordinate taxa is corroborated. While the evolution of ocelli was estimated to be dependent on flight capability, ocelli are yet absent in the majority of all winged species and only appear in members of few subordinate clades, which substantiates the hypothesis on their regain and thus on evolutionary trait reacquisition in general.

Publications

• Biodiversity of Phasmatodea. Insect Biodiversity, 281-313. Wiley.
  Bradler, Sven & Buckley, Thomas R.
  
• Evolution of Oviposition Techniques in Stick and Leaf Insects (Phasmatodea). Frontiers in Ecology and Evolution, 6.
  Robertson, James A.; Bradler, Sven & Whiting, Michael F.
  
• The Evolution of Tarsal Adhesive Microstructures in Stick and Leaf Insects (Phasmatodea). Frontiers in Ecology and Evolution, 6.
  Büscher, Thies H.; Buckley, Thomas R.; Grohmann, Constanze; Gorb, Stanislav N. & Bradler, Sven
  
• Old World and New World Phasmatodea: Phylogenomics Resolve the Evolutionary History of Stick and Leaf Insects. Frontiers in Ecology and Evolution, 7.
  Simon, Sabrina; Letsch, Harald; Bank, Sarah; Buckley, Thomas R.; Donath, Alexander; Liu, Shanlin; Machida, Ryuichiro; Meusemann, Karen; Misof, Bernhard; Podsiadlowski, Lars; Zhou, Xin; Wipfler, Benjamin & Bradler, Sven
  
• Tarsal attachment pads in Phasmatodea (Hexapoda: Insecta). Zoologica 164: 1–94. 2019
  Büscher T. H., Grohmann C., Bradler S. & Gorb S. N.
  
• When Giant Stick Insects Play With Colors: Molecular Phylogeny of the Achriopterini and Description of Two New Splendid Species (Phasmatodea: Achrioptera) From Madagascar. Frontiers in Ecology and Evolution, 7.
  Glaw, Frank; Hawlitschek, Oliver; Dunz, Andreas; Goldberg, Julia & Bradler, Sven
  
• Editorial: Stick Insect Research in the Era of Genomics: Exploring the Evolution of a Mesodiverse Insect Order. Frontiers in Ecology and Evolution, 8.
  Bradler, Sven & Buckley, Thomas R.
  
• Notes on the leaf insects of the genus Phyllium of Sumatra and Java, Indonesia, including the description of two new species with purple coxae (Phasmatodea, Phylliidae). ZooKeys, 913, 89-126.
  Cumming, Royce T.; Bank, Sarah; Le Tirant, Stephane & Bradler, Sven
  
• A tree of leaves: Phylogeny and historical biogeography of the leaf insects (Phasmatodea: Phylliidae). Communications Biology, 4(1).
  Bank, Sarah; Cumming, Royce T.; Li, Yunchang; Henze, Katharina; Le Tirant, Stéphane & Bradler, Sven
  
• Cryptophyllium, the hidden leaf insects – descriptions of a new leaf insect genus and thirteen species from the former celebicum species group (Phasmatodea, Phylliidae). ZooKeys, 1018, 1-179.
  Cumming, Royce T.; Bank, Sarah; Bresseel, Joachim; Constant, Jérôme; Le Tirant, Stéphane; Dong, Zhiwei; Sonet, Gontran & Bradler, Sven
  
• Reconstructing the nonadaptive radiation of an ancient lineage of ground‐dwelling stick insects (Phasmatodea: Heteropterygidae). Systematic Entomology, 46(3), 487-507.
  Bank, Sarah; Buckley, Thomas R.; Büscher, Thies H.; Bresseel, Joachim; Constant, Jérôme; de Haan, Mayk; Dittmar, Daniel; Dräger, Holger; Kahar, Rafhiah S.; Kang, Albert; Kneubühler, Bruno; Langton‐Myers, Shelley S. & Bradler, Sven
  
• A second view on the evolution of flight in stick and leaf insects (Phasmatodea). BMC Ecology and Evolution, 22(1).
  Bank, Sarah & Bradler, Sven
  
• PHASMATODEA, STICK AND LEAF INSECTS. The New Natural History of Madagascar, 1189-1201. Princeton University Press.
  Cliquennois, N. & Bradler, S.
  
• Divergence time and environmental similarity predict the strength of morphological convergence in stick and leaf insects. Cold Spring Harbor Laboratory.
  Boisseau, Romain P.; Bradler, Sven & Emlen, Douglas J.
  
• Leaves that walk and eggs that stick: comparative functional morphology and evolution of the adhesive system of leaf insect eggs (Phasmatodea: Phylliidae). BMC Ecology and Evolution, 23(1).
  Büscher, Thies H.; Bank, Sarah; Cumming, Royce T.; Gorb, Stanislav N. & Bradler, Sven
  
• On seven undescribed leaf insect species revealed within the recent “Tree of Leaves” (Phasmatodea, Phylliidae). ZooKeys, 1173, 145-229.
  Cumming, Royce T.; Le Tirant, Stéphane; Linde, Jackson B.; Solan, Megan E.; Foley, Evelyn Marie; Eulin, Norman Enrico C.; Lavado, Ramon; Whiting, Michael F.; Bradler, Sven & Bank, Sarah
  
• High disparity in repellent gland anatomy across major lineages of stick and leaf insects (Insecta: Phasmatodea). BMC Zoology, 9(1).
  Niekampf, Marco; Meyer, Paul; Quade, Felix S. C.; Schmidt, Alexander R.; Salditt, Tim & Bradler, Sven