Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings

Almudí, Isabel; Vizueta, Joel; Wyatt, Christopher D R; Mendoza, Alex de; Marlétaz, Ferdinand; Firbas, Panos; Feuda, Roberto; Masiero, Giulio; P, Medina; Alcaina-Caro, Ana; Cruz, Fernando; Gómez‐Garrido, Jèssica; Gut, Marta; Alioto, Tyler; Vargas-Chávez, Carlos; Davie, Kristofer; Misof, Bernhard; González, Josefa; Aerts, Stein; Lister, Ryan; Paps, Jordi; Rozas, Julio; Sánchez-Gracia, Alejandro; Irimia, Manuel; Maeso, Ignacio; Casares, Fernando

doi:10.1038/s41467-020-16284-8

Cited by 82 publications

(62 citation statements)

References 78 publications

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“…Niwa et al (2010) found that some wing genes are indeed expressed in these tissues. More recently, Almudi et al (2020) demonstrated a large overlap in the transcriptome of wings and abdominal gills in the mayfly Cloeon dipterum . The developmental origin of these abdominal tissues (specifically whether they are of tergal or pleural origin) and their Hox regulation have yet to be explored.…”

Section: Discussionmentioning

confidence: 99%

Tergal and pleural wing‐related tissues in the German cockroach and their implication to the evolutionary origin of insect wings

Clark-Hachtel

Fernández-Nicolas

Bellés

et al. 2021

Evolution and Development

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The acquisition of wings has facilitated the massive evolutionary success of pterygotes (winged insects), which now make up nearly three‐quarters of described metazoans. However, our understanding of how this crucial structure has evolved remains quite elusive. Historically, two ideas have dominated in the wing origin debate, one placing the origin in the dorsal body wall (tergum) and the other in the lateral pleural plates and the branching structures associated with these plates. Through studying wing‐related tissues in the wingless segments (such as wing serial homologs) of the beetle, Tribolium castaneum, we obtained several crucial pieces of evidence that support a third idea, the dual origin hypothesis, which proposes that wings evolved from a combination of tergal and pleural tissues. Here, we extended our analysis outside of the beetle lineage and sought to identify wing‐related tissues from the wingless segments of the cockroach, Blattella germanica. Through detailed functional and expression analyses for a critical wing gene, vestigial (vg), along with re‐evaluating the homeotic transformation of a wingless segment induced by an improved RNA interference protocol, we demonstrate that B. germanica possesses two distinct tissues in their wingless segments, one with tergal and one with pleural nature, that might be evolutionarily related to wings. This outcome appears to parallel the reports from other insects, which may further support a dual origin of insect wings. However, we also identified a vg‐independent tissue that contributes to wing formation upon homeotic transformation, as well as vg‐dependent tissues that do not appear to participate in wing formation, in B. germanica, indicating a more complex evolutionary history of the tissues that contributed to the emergence of insect wings.

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Section: Discussionmentioning

confidence: 99%

Tergal and pleural wing‐related tissues in the German cockroach and their implication to the evolutionary origin of insect wings

Clark-Hachtel

Fernández-Nicolas

Bellés

et al. 2021

Evolution and Development

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“…For all insects (including mosquitoes), the mean genome size in the Animal Genome Size Database is 1077 Mbp ( n = 1345; accessed 13 July 2020) [ 26 ]. While aquatic insects are poorly represented in the Animal Genome Size Database, sequencing-based reports of their genome sizes include five taxonomic orders with a mean size of 600 Mbp ( n = 20) [ 27 , 28 , 29 , 30 , 31 ]. Thus, there is no evidence that aquatic insect genomes are particularly large and unwieldy when compared to their terrestrial counterparts.…”

Section: Resultsmentioning

confidence: 99%

Aquatic Insects Are Dramatically Underrepresented in Genomic Research

Hotaling

Kelley

Frandsen

2020

Insects

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Aquatic insects comprise 10% of all insect diversity, can be found on every continent except Antarctica, and are key components of freshwater ecosystems. However, aquatic insect genome biology lags dramatically behind that of terrestrial insects. If genomic effort was spread evenly, one aquatic insect genome would be sequenced for every ~9 terrestrial insect genomes. Instead, ~24 terrestrial insect genomes have been sequenced for every aquatic insect genome. This discrepancy is even more dramatic if the quality of genomic resources is considered; for instance, while no aquatic insect genome has been assembled to the chromosome level, 29 terrestrial insect genomes spanning four orders have. We argue that a lack of aquatic insect genomes is not due to any underlying difficulty (e.g., small body sizes or unusually large genomes), yet it is severely hampering aquatic insect research at both fundamental and applied scales. By expanding the availability of aquatic insect genomes, we will gain key insight into insect diversification and empower future research for a globally important taxonomic group.

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“…For all insects (including mosquitoes), the mean genome size in the Animal Genome Size Database is 1077 Mbp (n = 1,345; accessed 13 July 2020) [22]. While aquatic insects are poorly represented in the Animal Genome Size Database, sequencing-based reports of their genome sizes include five taxonomic orders with a mean size of 600 Mbp (n = 20) [23][24][25][26][27]. Thus, there is no evidence that aquatic insect genomes are particularly large and unwieldy when compared to their terrestrial counterparts.…”

Section: Resultsmentioning

confidence: 99%

Aquatic insects are dramatically underrepresented in genomic research

Hotaling

Kelley

Frandsen

2020

Preprint

View full text Add to dashboard Cite

Aquatic insects comprise 10% of all insect diversity, can be found on every continent except Antarctica, and are key components of freshwater ecosystems. Yet aquatic insect genome biology lags dramatically behind that of terrestrial insects. If genomic effort was spread evenly, one aquatic insect genome would be sequenced for every ~9 terrestrial insect genomes. Instead, ~24 terrestrial insect genomes have been sequenced for every aquatic insect genome. This discrepancy is even more dramatic if the quality of genomic resources is considered; for instance, while no aquatic insect genome has been assembled to the chromosome level, 29 terrestrial insect genomes spanning four orders have. We argue that a lack of aquatic insect genomes is not due to any underlying difficulty (e.g., small body sizes or unusually large genomes) yet it is severely hampering aquatic insect research at both fundamental and applied scales. By expanding the availability of aquatic insect genomes, we will gain key insight into insect diversification and empower future research for a globally important taxonomic group.

show abstract

Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings

Cited by 82 publications

References 78 publications

Tergal and pleural wing‐related tissues in the German cockroach and their implication to the evolutionary origin of insect wings

Tergal and pleural wing‐related tissues in the German cockroach and their implication to the evolutionary origin of insect wings

Aquatic Insects Are Dramatically Underrepresented in Genomic Research

Aquatic insects are dramatically underrepresented in genomic research

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