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Structural mouthpart interaction evolved already in the earliest lineages of insects


Blanke, Alexander; Rühr, Peter T; Mokso, Rajmund; Villanueva, Pablo; Wilde, Fabian; Stampanoni, Marco; Uesugi, Kentaro; Machida, Ryuichiro; Misof, Bernhard (2015). Structural mouthpart interaction evolved already in the earliest lineages of insects. Proceedings of the Royal Society of London, Series B: Biological Sciences, 282(1812):20151033.

Abstract

In butterflies, bees, flies and true bugs specific mouthparts are in close contact or even fused to enable piercing, sucking or sponging of particular food sources. The common phenomenon behind these mouthpart types is a complex composed of several consecutive mouthparts which structurally interact during food uptake. The single mouthparts are thus only functional in conjunction with other adjacent mouthparts, which is fundamentally different to biting-chewing. It is, however, unclear when structural mouthpart interaction (SMI) evolved since this principle obviously occurred multiple times independently in several extant and extinct winged insect groups. Here, we report a new type of SMI in two of the earliest wingless hexapod lineages--Diplura and Collembola. We found that the mandible and maxilla interact with each other via an articulatory stud at the dorsal side of the maxillary stipes, and they are furthermore supported by structures of the hypopharynx and head capsule. These interactions are crucial stabilizing elements during food uptake. The presence of SMI in these ancestrally wingless insects, and its absence in those crustacean groups probably ancestral to insects, indicates that SMI is a groundplan apomorphy of insects. Our results thus contradict the currently established view of insect mouthpart evolution that biting-chewing mouthparts without any form of SMI are the ancestral configuration. Furthermore, SMIs occur in the earliest insects in a high anatomical variety. SMIs in stemgroup representatives of insects may have triggered efficient exploitation and fast adaptation to new terrestrial food sources much earlier than previously supposed.

Abstract

In butterflies, bees, flies and true bugs specific mouthparts are in close contact or even fused to enable piercing, sucking or sponging of particular food sources. The common phenomenon behind these mouthpart types is a complex composed of several consecutive mouthparts which structurally interact during food uptake. The single mouthparts are thus only functional in conjunction with other adjacent mouthparts, which is fundamentally different to biting-chewing. It is, however, unclear when structural mouthpart interaction (SMI) evolved since this principle obviously occurred multiple times independently in several extant and extinct winged insect groups. Here, we report a new type of SMI in two of the earliest wingless hexapod lineages--Diplura and Collembola. We found that the mandible and maxilla interact with each other via an articulatory stud at the dorsal side of the maxillary stipes, and they are furthermore supported by structures of the hypopharynx and head capsule. These interactions are crucial stabilizing elements during food uptake. The presence of SMI in these ancestrally wingless insects, and its absence in those crustacean groups probably ancestral to insects, indicates that SMI is a groundplan apomorphy of insects. Our results thus contradict the currently established view of insect mouthpart evolution that biting-chewing mouthparts without any form of SMI are the ancestral configuration. Furthermore, SMIs occur in the earliest insects in a high anatomical variety. SMIs in stemgroup representatives of insects may have triggered efficient exploitation and fast adaptation to new terrestrial food sources much earlier than previously supposed.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > Institute of Biomedical Engineering
Dewey Decimal Classification:170 Ethics
610 Medicine & health
Uncontrolled Keywords:Collembola; Diplura; entognathy; functional morphology; microCT
Language:English
Date:2015
Deposited On:09 Feb 2016 11:03
Last Modified:05 Apr 2016 20:00
Publisher:Royal Society Publishing
ISSN:0962-8452
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1098/rspb.2015.1033
PubMed ID:26203002

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