A morphological novelty evolved by co-option of a reduced gene regulatory network and gene recruitment in a beetle

Hu, Yonggang; Schmitt-Engel, Christian; Schwirz, Jonas; Stroehlein, Nadi; Richter, Tobias; Majumdar, Upalparna; Bucher, Gregor

doi:10.1098/rspb.2018.1373

Cited by 28 publications

(37 citation statements)

References 64 publications

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“…In the telotrophic ovary type of Tribolium the biology of somatic stem cells can be studied independent of germline stem cells, which cease to divide prior to hatching [9]. Tribolium is also studied with respect to beetle specific evolutionary novelties such as elytra [10] and gin traps [11]. It is also amenable to studies of physiology such as the formation of the extremely hard cuticle [12], and the function of the cryptonephridial system [13], which is a model for unique adaptation to dry habitats.…”

Section: Introductionmentioning

confidence: 99%

Enhanced genome assembly and a new official gene set for Tribolium castaneum

et al. 2020

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Background: The red flour beetle Tribolium castaneum has emerged as an important model organism for the study of gene function in development and physiology, for ecological and evolutionary genomics, for pest control and a plethora of other topics. RNA interference (RNAi), transgenesis and genome editing are well established and the resources for genome-wide RNAi screening have become available in this model. All these techniques depend on a high quality genome assembly and precise gene models. However, the first version of the genome assembly was generated by Sanger sequencing, and with a small set of RNA sequence data limiting annotation quality. Results: Here, we present an improved genome assembly (Tcas5.2) and an enhanced genome annotation resulting in a new official gene set (OGS3) for Tribolium castaneum, which significantly increase the quality of the genomic resources. By adding large-distance jumping library DNA sequencing to join scaffolds and fill small gaps, the gaps in the genome assembly were reduced and the N50 increased to 4753kbp. The precision of the gene models was enhanced by the use of a large body of RNA-Seq reads of different life history stages and tissue types, leading to the discovery of 1452 novel gene sequences. We also added new features such as alternative splicing, well defined UTRs and microRNA target predictions. For quality control, 399 gene models were evaluated by manual inspection. The current gene set was submitted to Genbank and accepted as a RefSeq genome by NCBI. Conclusions: The new genome assembly (Tcas5.2) and the official gene set (OGS3) provide enhanced genomic resources for genetic work in Tribolium castaneum. The much improved information on transcription start sites supports transgenic and gene editing approaches. Further, novel types of information such as splice variants and microRNA target genes open additional possibilities for analysis.

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Section: Introductionmentioning

confidence: 99%

Enhanced genome assembly and a new official gene set for Tribolium castaneum

et al. 2020

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“…It refers to several independent underlying processes that lead to similar appearing morphologies. Yet, these may represent: (1) true independent novelties; (2) characters that were present in early representatives of the lineage, then lost in later forms, but then 'reactivated' in deeply nested ingroups; (3) repetitive expression of characters that seem to be present as potential from a genetic basis already in early ancestors (Hu et al, 2018).…”

Section: Convergence As a Major Factor For Form Diversitymentioning

confidence: 99%

An unusual 100-million-year old holometabolan larva with a piercing mouth cone

Haug

Schädel

Baranov

et al. 2020

PeerJ

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Holometabola is a hyperdiverse group characterised by a strong morphological differentiation between early post-embryonic stages (= larvae) and adults. Adult forms of Holometabola, such as wasps, bees, beetles, butterflies, mosquitoes or flies, are strongly differentiated concerning their mouth parts. The larvae most often seem to retain rather plesiomorphic-appearing cutting-grinding mouth parts. Here we report a new unusual larva preserved in Burmese amber. Its mouth parts appear beak-like, forming a distinct piercing mouth cone. Such a morphology is extremely rare among larval forms, restricted to those of some beetles and lacewings. The mouth parts of the new fossil are forward oriented (prognathous). Additionally, the larva has distinct subdivisions of tergites and sternites into several sclerites. Also, the abdomen segments bear prominent protrusions. We discuss this unusual combination of characters in comparison to the many different types of holometabolan larvae. The here reported larva is a new addition to the ‘unusual zoo’ of the Cretaceous fauna including numerous, very unusual appearing forms that have gone extinct at the Cretaceous–Palaeogene boundary.

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“…Taken together, these results show that the Hedgehog circuit is flexible over time and emphasize the possibility that en is coopted partly independently from its wing disc network in S. leonensis to its novel expression pattern prefiguring the wing white spots. Examples of partial GRN recruitment are scarce, but such molecular events have been proposed to underlie the development of abdominal appendages in sepsid flies (72,73), the formation of eyespots in butterflies (74,75), and the origin of gin-trap in beetle pupae (76).…”

Section: Late Redeployment Of Engrailed Does Not Affect Wing Morpholomentioning

confidence: 99%

Temporal flexibility of gene regulatory network underlies a novel wing pattern in flies

Dufour

Koshikawa

Finet

2020

Proc. Natl. Acad. Sci. U.S.A.

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Organisms have evolved endless morphological, physiological, and behavioral novel traits during the course of evolution. Novel traits were proposed to evolve mainly by orchestration of preexisting genes. Over the past two decades, biologists have shown that cooption of gene regulatory networks (GRNs) indeed underlies numerous evolutionary novelties. However, very little is known about the actual GRN properties that allow such redeployment. Here we have investigated the generation and evolution of the complex wing pattern of the flySamoaia leonensis. We show that the transcription factor Engrailed is recruited independently from the other players of the anterior–posterior specification network to generate a new wing pattern. We argue that partial cooption is made possible because 1) the anterior–posterior specification GRN is flexible over time in the developing wing and 2) this flexibility results from the fact that every single gene of the GRN possesses its own functional time window. We propose that the temporal flexibility of a GRN is a general prerequisite for its possible cooption during the course of evolution.

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A morphological novelty evolved by co-option of a reduced gene regulatory network and gene recruitment in a beetle

Cited by 28 publications

References 64 publications

Enhanced genome assembly and a new official gene set for Tribolium castaneum

Enhanced genome assembly and a new official gene set for Tribolium castaneum

An unusual 100-million-year old holometabolan larva with a piercing mouth cone

Temporal flexibility of gene regulatory network underlies a novel wing pattern in flies

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