The earliest known holometabolous insects

Nel, André; Roques, Patrick; Nel, Patricia; Прокин, А. А.; Bourgoin, Thierry; Prokop, Jakub; Szwedo, Jacek; Azar, Dany; Desutter‐Grandcolas, Laure; Wappler, Torsten; Garrouste, Romain; Coty, David; Huang, Diying; Engel, Michael S.; Kirejtshuk, Alexander G.

doi:10.1038/nature12629

Cited by 162 publications

(118 citation statements)

References 26 publications

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“…Ultrabithorax, Engrailed, Cubitus Interruptus and Apterous proteins are all seen in butterflies in patterns very similar to their known role in flies [19][20][21][22][23]. It seems likely, therefore, that early events in the development of the wing have been conserved throughout the evolution of holometabolous insects, over some 300 Myr of evolution [24].…”

Section: Early Wing Development In the Flymentioning

confidence: 90%

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

Jiggins¹,

Wallbank²,

Hanly³

2017

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. A major challenge is to understand how conserved gene regulatory networks control the wonderful diversity of form that we see among animals and plants. Butterfly wing patterns are an excellent example of this diversity. Butterfly wings form as imaginal discs in the caterpillar and are constructed by a gene regulatory network, much of which is conserved across the holometabolous insects. Recent work in Heliconius butterflies takes advantage of genomic approaches and offers insights into how the diversification of wing patterns is overlaid onto this conserved network. WntA is a patterning morphogen that alters spatial information in the wing. Optix is a transcription factor that acts later in development to paint specific wing regions red. Both of these loci fit the paradigm of conserved protein-coding loci with diverse regulatory elements and developmental roles that have taken on novel derived functions in patterning wings. These discoveries offer insights into the 'Nymphalid Ground Plan', which offers a unifying hypothesis for pattern formation across nymphalid butterflies. These loci also represent 'hotspots' for morphological change that have been targeted repeatedly during evolution. Both convergent and divergent evolution of a great diversity of patterns is controlled by complex alleles at just a few genes. We suggest that evolutionary change has become focused on one or a few genetic loci for two reasons. First, pre-existing complex cis-regulatory loci that already interact with potentially relevant transcription factors are more likely to acquire novel functions in wing patterning. Second, the shape of wing regulatory networks may constrain evolutionary change to one or a few loci. Overall, genomic approaches that have identified wing patterning loci in these butterflies offer broad insight into how gene regulatory networks evolve to produce diversity.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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Section: Early Wing Development In the Flymentioning

confidence: 90%

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

Jiggins¹,

Wallbank²,

Hanly³

2017

Phil. Trans. R. Soc. B

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“…The fossil record shows now that the holometabolous insects were already present during the early Late Carboniferous with representatives of the mecopteran, hymenopteran, and coleopteran clades [3].…”

Section: The Holometaboly: a Crucial Innovation But With Delayed Conmentioning

confidence: 99%

“…Some were very small (less than 4 mm long), even if they have been generally neglected by fossil collectors and have been collected only in these last few years [3].…”

Section: Were the Carboniferous Insects All Giant?mentioning

confidence: 99%

“…These localities provided very rich and diverse entomofaunas, with species belonging to extant taxa (cockroaches including the diverse Carboniferous Paoliida, Orthoptera or grasshoppers, Odonatoptera or dragonflies, etc. ), but also other that correspond to extinct, strictly 00006-p. 3 Palaeozoic groups, the most famous one being the Palaeodictyoptera [2]. Our knowledge on these earliest winged insects has greatly increased during these last years.…”

Section: Did the Insect Diversity Increase Progressively From The Carmentioning

confidence: 99%

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Some misconceptions or preconceived ideas on the history of the Insects

Nel

2015

BIO Web of Conferences

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Abstract. The Hexapoda is the most diverse clade of the history of life. They cannot be considered as the oldest terrestrial animals and the first Hexapoda were small apterous animals of the Devonian soil fauna, apparently not very diverse and "dominated" by myriapods and arachnids at that time. Things dramatically changed during the Early Carboniferous with the appearance and the expansion of the winged insects. This crucial innovation allowed this clade to diversify in a spectacular way in the Late Carboniferous. The main clades were already present at the end of this period, viz. Palaeoptera, "Polyneoptera", Paraneoptera and Holometabola. The latter two groups became truly diverse and began to dominate the animal kingdom after the major Permo-Triassic biodiversity crisis. Nevertheless a causal link is difficult to establish between the two phenomena. After the Triassic, all insect orders are present and many modern families are as old as the Jurassic, a situation completely different from that of the terrestrial vertebrates. The last major change in the hexapods took place about 100 Ma ago, and may be linked with the mid-Cretaceous angiosperm diversification, but apparently not with the supposed major crisis of diversity at the end of the Cretaceous.

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“…340-280 Ma [47]) and the radiation of flowering plants (approx. 120-70 Ma [48,49]). Likewise, a correlation of the piercing-sucking functional mouthpart unit with the appearance of non-symbiotic terrestrial fungi [29,50] or bryophytes [46] in the mid-Ordovician is a likely scenario given the potential origin and diversification of Collembola and Diplura at the same time as indicated by recent dating analyses (figure 2) [11].…”

Section: (C) the Evolution Of Structural Mouthpart Interactions In Inmentioning

confidence: 99%

Structural mouthpart interaction evolved already in the earliest lineages of insects

et al. 2015

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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 lineagesDiplura 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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The earliest known holometabolous insects

Cited by 162 publications

References 26 publications

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

Some misconceptions or preconceived ideas on the history of the Insects

Structural mouthpart interaction evolved already in the earliest lineages of insects

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