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Home , Evolution of insects, Insect wing, Metapterygota, Neoptera, Palaeoptera, Polyneoptera

BriefGuide A Brief Guide to the of flying

Sabrina Simon

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Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, NY, USA

Corresponding author: Sabrina Simon E-mail: [email protected]

The evolutionary novelty – – ignited the mega-diversity and evolutionary success of insects and is one of the most fascinating issues in developmental and . However, neither the origin of insect wings nor the early evolution of winged insects () is well understood.

Origin of insect wings The origin of insect wings can be explained by two main hypotheses: insect wings represent a novel structure (Paranotal hypothesis) or a modification of an existing structure ( branch hypothesis) [1]. Based on the Paranotal hypothesis, wings evolved as novel outgrowths of the thoracic tergum, or paranotal lobe, as an adaption to gliding prior to the appearance of proper wings [2] (Figure 1a). The second hypothesis proposes that wings Figure 1. a) Colored: shown are the proposed structural homologies according to the two main hypotheses for the evolutionary origin of are a modification of limb branches that were insect wings. Based on the Paranotal hypothesis the paranotal lobes present in ancestral branched of their (non-articulated) existing in the extinct Paleodictyoptera are homologous to the functional wings in modern insects. In contrast, ancestors and served as respiratory surfaces the Limb branch hypothesis considers the observed in (gills) before modification into powerful nymphs for respiration as homologous structures to insect wings. b) Proposed phylogenetic relationships for the earliest branching organs [3]. lineages of Pterygota: Pala, ; Meta, ; and Both hypotheses are supported by developmental Chias, Chiastomyaria hypothesis. studies of regulatory but have been ques- tioned for various reasons. The Paranotal hypo-

thesis is implausible in a parsimonious evolu- Keywords: insect evolution; ; wings; folding

Please note: this contribution was not peer-reviewed. 1 tionary scenario – the derivation of mobile (all other extant insects with wing flexion) structures (flapping wings) from primitively (Figure 1b). Here, a major problem is the immobile paranotal lobes. This suggests assignment of between the primarily secondarily derived wing articulation but the origin wingless outgroup () and the winged of muscles allowing flapping movement remains insects for several characters related to the wings, unclear. In contrast, the Limb branch hypothesis e.g. thoracic muscles, muscles related to flight presumes that wings evolved in aquatic habitats. apparatus. However, recent head structure Based on the record, winged insects analyses revived the Palaeoptera hypothesis – a probably had a terrestrial origin and the different sister-group relationship between and adaptions of aquatic nymphs seen in winged (+Ephemeroptera, Neoptera) [7]. insects indicate a secondarily independent In contrast, establishing a sound phylogenetic colonization of aquatic habitats [4]. Paleontological hypothesis for the evolution of flying insects based evidence is limited in terms of addressing the on molecular data sets is problematic even in the question of morphological and functional origin of phylogenomic era, resulting in striking dis- insect wings. No fossil record is known with agreements; see [8, 9] and references therein. intermediate winged stages and the oldest Additionally, the elucidation of the origin of wing presumably winged insect fossil is 45 million years folding – another evolutionary novelty with critical (My) younger than primarily wingless ancestors importance for insect radiation – remains (411.5 My) [5]. However, expression studies of challenging. Within Neoptera three infraclasses three wing-regulatory genes in a mayfly have been proposed based on morphological (Ephemeroptera) and a wingless bristletail insect characters: (lower neopteran insects; () proposed a combinatorial , mantids, , stoneflies, etc.), developmental model for wing origin where the (, lice, bugs in the wide sense) thoracic tergal edge (paranotal lobe) is the putative and Holometabola (insects undergoing complete source of wing margin formation [6]. ; , , , etc.). While the of the latter two is well Early evolution of winged insects established based on morphological and molecular Knowledge of the evolution of the earliest analyses, evidence for monophyletic Polyneoptera pterygote lineages is critical to understanding what has only slightly increased in the past. Analyses of ancestral structure wings evolved from. The wing base structures [10] and large transcriptomic traditional view separating Pterygota into two data sets [8, 11] consistently provide support for monophyletic – Palaeoptera and Neoptera, this grouping, while e.g. rRNA analyses, still based on the ability or inability of wing folding – favor a paraphyletic lower neopteran group as the has been disproved based on different sets of common ancestor of wing folding in Neoptera. The morphological characters. Indeed, morphological “ancient rapid radiation” [12] of the insects, their characters have provided strong support for all mega-diversity [13] and the preserved ancient three possible branching patterns between the two characters in some taxa [14] might all be extant palaeopterous orders – Ephemeroptera contributing factors which complicate a robust (mayflies) and Odonata (dragon- and ) resolution of insect relationships and consequently (both unable to fold wings over ) – and hamper the elucidation of evolution.

Please note: this contribution was not peer-reviewed. 2

Acknowledgements This work was supported by a fellowship within the Postdoc-Program of the German Academic Exchange Service (DAAD). Special thanks go also to Rob DeSalle, my supervisor, who carefully checked this article.

References

1. Jockusch EL, Ober KA. 2004. Hypothesis testing incongruence using new transcriptomic data. in evolutionary : A case study Genome Biol Evol 4: 1295-309. from insect wings. J Hered 95: 382-96. 9. Simon S, Strauss S, von Haeseler A, Hadrys H. 2. Hamilton KGA. 1971. The insect wing, Pt. 1. 2009. A phylogenomic approach to resolve the Origin and development of wings from notal lobes. J basal pterygote divergence. Mol Biol Evol 26: 2719- Kansas Entomol Soc 44: 421-33. 30. 3. Averof M, Cohen SM. 1997. Evolutionary origin of 10. Yoshizawa K. 2011. Monophyletic Polyneoptera insect wings from ancestral gills. 385: 627- recovered by wing base structure. Syst Entomol 36: 30. 377-94. 4. Grimaldi DA, Engel MS. 2005. Evolution of the 11. Letsch HO, Meusemann K, Wipfler B, Schutte K, Insects New York: Cambridge University Press. et al. 2012. Insect phylogenomics: results, problems 5. Garrouste R, Clement G, Nel P, Engel MS, et al. and the impact of matrix composition. Proc Biol Sci 2012. A complete insect from the Late 279: 3282-90. period. Nature 488: 82-5. 12. Whitfield JB, Kjer KM. 2008. Ancient rapid 6. Niwa N, Akimoto-Kato A, Niimi T, Tojo K, et al. radiations of insects: challenges for phylogenetic 2010. Evolutionary origin of the insect wing via analysis. Annu Rev Entomol 53: 449-72. integration of two developmental modules. Evol Dev 13. Yeates DK, Cameron SL, Trautwein M. 2012. A 12: 168-76. view from the edge of the forest: recent progress in 7. Blanke A, Wipfler B, Letsch H, Koch M, et al. understanding the relationships of the insect orders. 2012. Revival of Palaeoptera—head characters Aust J Entomol 51: 79-87. support a monophyletic origin of Odonata and 14. Willmann R. 2004. Phylogenetic Relationships and Ephemeroptera (Insecta). 28: 560-81. . In Cracraft J, Donoghue MJ, 8. Simon S, Narechania A, Desalle R, Hadrys H. eds. Assembling the Tree of : Oxford University 2012. Insect phylogenomics: exploring the source of Press. p 330-44.