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Establishment of the mayfly Cloeon dipterum as a new model system to investigate insect evolution.

ABSTRACT: The great capability of insects to adapt to new environments promoted their extraordinary diversification, resulting in the group of Metazoa with the largest number of species distributed worldwide. To understand this enormous diversity, it is essential to investigate lineages that would allow the reconstruction of the early events in the evolution of insects. However, research on insect ecology, physiology, development and evolution has mostly focused on few well-established model species. The key phylogenetic position of mayflies within Paleoptera as the sister group of the rest of winged insects and life history traits of mayflies make them an essential order to understand insect evolution. Here, we describe the establishment of a continuous culture system of the mayfly Cloeon dipterum and a series of experimental protocols and omics resources that allow the study of its development and its great regenerative capability. Thus, the establishment of Cloeon as an experimental platform paves the way to understand genomic and morphogenetic events that occurred at the origin of winged insects.

SUBMITTER: Almudi I

PROVIDER: S-EPMC6446309 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Establishment of the mayfly <i>Cloeon dipterum</i> as a new model system to investigate insect evolution.

Almudi Isabel I Martín-Blanco Carlos A CA García-Fernandez Isabel M IM López-Catalina Adrián A Davie Kristofer K Aerts Stein S Casares Fernando F

EvoDevo 20190402

The great capability of insects to adapt to new environments promoted their extraordinary diversification, resulting in the group of Metazoa with the largest number of species distributed worldwide. To understand this enormous diversity, it is essential to investigate lineages that would allow the reconstruction of the early events in the evolution of insects. However, research on insect ecology, physiology, development and evolution has mostly focused on few well-established model species. The ...[more]

PMID: 30984364

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Project description:BackgroundHox genes are key regulators of appendage development in the insect body plan. The body plan of mayfly (Ephemeroptera) nymphs differs due to the presence of abdominal appendages called gills. Despite mayflies' phylogenetic position in Paleoptera and novel morphology amongst insects, little is known of their developmental genetics, such as the appendage-regulating Hox genes. To address this issue we present an annotated, early instar transcriptome and embryonic expression profiles for Antennapedia, Ultrabithorax, and Abdominal A proteins in the mayfly Hexagenia limbata, identify putative Hox protein sequences in the mayflies H. limbata, Cloeon dipterum, and Ephemera danica, and describe the genomic organization of the Hox gene cluster in E. danica.ResultsTranscriptomic sequencing of early instar H. limbata nymphs yielded a high-quality assembly of 83,795 contigs, of which 22,975 were annotated against Folsomia candida, Nilaparvata lugens, Zootermopsis nevadensis and UniRef90 protein databases. Homeodomain protein phylogeny and peptide annotations identified coding sequences for eight of the ten canonical Hox genes (excluding zerknüllt/Hox3 and fushi tarazu) in H. limbata and C. dipterum, and all ten in E. danica. Mayfly Hox protein sequences and embryonic expression patterns of Antp, Ubx, and Abd-A appear highly conserved with those seen in other non-holometabolan insects. Similarly, the genomic organization of the Hox cluster in E. danica resembles that seen in most insects.ConclusionsWe present evidence that mayfly Hox peptide sequences and the embryonic expression patterns for Antp, Ubx, and Abd-A are extensively conserved with other insects, as is organization of the mayfly Hox gene cluster. The protein data suggest mayfly Antp, Ubx, and Abd-A play appendage promoting and repressing roles during embryogenesis in the thorax and abdomen, respectively, as in other insects. The identified expression of eight Hox genes, including Ubx and abd-A, in early instar nymphs further indicates a post-embryonic role, possibly in gill development. These data provide a basis for H. limbata as a complementary Ephemeridae model to the growing repertoire of mayfly model species and molecular techniques.

Project description:The family Baetiscidae Edmunds & Traver, 1954 is recognisable among mayflies due to its bizarre larvae, equipped with a robust and spiked thoracic notal shield covering part of the abdomen up to sixth segment. Originally being described as extant species from the USA and Canada, Baetiscidae were later found in the fossil record as well, specifically in Cretaceous of Brazil and Eocene Baltic amber. An enigmatic piece of fossil evidence are two larvae from the Early Cretaceous Koonwarra Fossil Bed in Australia, which have been presumed as attributable to Baetiscidae and briefly discussed in previous studies. In the present contribution, we reinvestigate these fossils and confirm their attribution to the family Baetiscidae. These larvae are depicted and described as Koonwarrabaetisca jelli gen. et sp. nov. and Koonwarrabaetisca duncani sp. nov. For both Cretaceous genera Protobaetisca Staniczek, 2007 and Koonwarrabaetisca gen. nov. we establish a new subfamily Protobaetiscinae subfam. nov. within the family Baetiscidae, based on the presence of markedly shortened thoracic sterna. The phylogenetic position of newly described subfamily is clarified using a cladistic analysis; Protobaetiscinae subfam. nov. forms a monophyletic clade, sister to Baetiscinae. The confirmation of the distribution of Baetiscidae in the Cretaceous of Australia suggests almost worldwide distribution of this family in the deep time. Given their limited dispersal abilities, this distributional pattern can be best explained by the Pangean origin for this family, moving the time of their origin at least to the Early Jurassic. The larvae of Koonwarrabaetisca gen. nov. exhibit the same ecomorphological specialization as the rest of Baetiscidae, that supporting with a high probability their lifestyle similar to extant Baetisca Walsh, 1862. The larvae probably lived in the flowing water with stony substrate densely covered by filamentous algae, and in the places of accumulation of dead plant and algae matter during the last instars. Thus, Koonwarrabaetisca gen. nov. could be the allochthonous component in mayfly fauna of the Koonwarra paleolake.

Project description:BACKGROUND:The ability to compose biological systems from smaller elements that act independently of the other upon assembly may help make the forward engineering of biological systems practical. Engineering biology in this manner is made difficult by the inherent nonlinear response of organisms to genetic devices. Devices are inevitably coupled to one another in the cell because they share the same transcriptional machinery for expression. Thus, new properties can emerge when devices that had been characterized in isolation are expressed concurrently. We show in this report that, similar to physical systems, the Escherichia coli (E. coli) transcriptional system can exhibit linear behavior under "small" perturbation conditions. This, in turn, allows devices to be treated as independent modules. RESULTS:We developed a framework and model system consisting of three devices to investigate linear system behavior in E. coli. Our framework employed the transfer curve concept to determine the amount of nonlinearity elicited by the E. coli transcriptional system in response to the devices. To this effect, the model system was quantitatively characterized using real-time quantitative PCR to produce device transfer curves (DTCs). Two of the devices encoded the bacterial neomycin phosphotransferase II (nptII) and chloramphenicol acetyl transferase (cat), while the third encoded the jellyfish-originating green fluorescent protein (gfp). The gfp device was the most nonlinear in our system, with nptII and cat devices eliciting linear responses. Superposition experiments verified these findings, with independence among the three devices having been lost when gfp was present at copy numbers above the lowest one used. CONCLUSIONS:We show that linear system behavior is possible in E. coli. Elucidation of the mechanism underlying the nonlinearity observed in gfp may lead to design rules that ensure linear system behavior, enabling the accurate prediction of the quantitative behavior of a system assembled from individually characterized devices. Our work suggests that biological systems follow principles similar to physical ones, and that concepts borrowed from the latter (such as DTCs) may be of use in the characterization and design of biological systems.

Dataset Information

Establishment of the mayfly Cloeon dipterum as a new model system to investigate insect evolution.

Publications

Establishment of the mayfly <i>Cloeon dipterum</i> as a new model system to investigate insect evolution.

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