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1. Wing serial homologues and the diversification of insect outgrowths: insights from the pupae of scarab beetles

   https://doi.org/10.1098/rspb.2020.2828  

   Hu, Yonggang; Moczek, Armin P. (January 2021, Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Modification of serially homologous structures is a common avenue towards functional innovation in developmental evolution, yet ancestral affinities among serial homologues may be obscured as structure-specific modifications accumulate over time. We sought to assess the degree of homology to wings of three types of body wall projections commonly observed in scarab beetles: (i) the dorsomedial support structures found on the second and third thoracic segments of pupae, (ii) the abdominal support structures found bilaterally in most abdominal segments of pupae, and (iii) the prothoracic horns which depending on species and sex may be restricted to pupae or also found in adults. We functionally investigated 14 genes within, as well as two genes outside, the canonical wing gene regulatory network to compare and contrast their role in the formation of each of the three presumed wing serial homologues. We found 11 of 14 wing genes to be functionally required for the proper formation of lateral and dorsal support structures, respectively, and nine for the formation of prothoracic horns. At the same time, we document multiple instances of divergence in gene function across our focal structures. Collectively, our results support the hypothesis that dorsal and lateral support structures as well as prothoracic horns share a developmental origin with insect wings. Our findings suggest that the morphological and underlying gene regulatory diversification of wing serial homologues across species, life stages and segments has contributed significantly to the extraordinary diversity of arthropod appendages and outgrowths. 

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2. Beetle horns evolved from wing serial homologs

   https://doi.org/10.1126/science.aaw2980  

   Hu, Yonggang; Linz, David M.; Moczek, Armin P. (November 2019, Science)

   Understanding how novel complex traits originate is a foundational challenge in evolutionary biology. We investigated the origin of prothoracic horns in scarabaeine beetles, one of the most pronounced examples of secondary sexual traits in the animal kingdom. We show that prothoracic horns derive from bilateral source tissues; that diverse wing genes are functionally required for instructing this process; and that, in the absence of Hox input, prothoracic horn primordia transform to contribute to ectopic wings. Once induced, however, the transcriptional profile of prothoracic horns diverges markedly from that of wings and other wing serial homologs. Our results substantiate the serial homology between prothoracic horns and insects wings and suggest that other insect innovations may derive similarly from wing serial homologs and the concomitant establishment of structure-specific transcriptional landscapes. 

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3. Multiple roles for laccase2 in butterfly wing pigmentation, scale development, and cuticle tanning

   https://doi.org/10.1111/ede.12338  

   Peng, Ceili L.; Mazo‐Vargas, Anyi; Brack, Benjamin J.; Reed, Robert D. (July 2020, Evolution & Development)

   Abstract Lepidopteran wing scales play important roles in a number of functions including color patterning and thermoregulation. Despite the importance of wing scales, however, we still have a limited understanding of the genetic mechanisms that underlie scale patterning, development, and coloration. Here, we explore the function of the phenoloxidase‐encoding genelaccase2in wing and scale development in the nymphalid butterflyVanessa cardui. Somatic deletion mosaics oflaccase2generated by CRISPR/Cas9 genome editing presented several distinct mutant phenotypes. Consistent with the work in other nonlepidopteran insect groups, we observed reductions in melanin pigmentation and defects in cuticle formation. We were also surprised, however, to see distinct effects on scale development including complete loss of wing scales. This study highlightslaccase2as a gene that plays multiple roles in wing and scale development and provides new insight into the evolution of lepidopteran wing coloration. 

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4. A large deletion at the cortex locus eliminates butterfly wing patterning

   https://doi.org/10.1093/g3journal/jkac021  

   Hanly, Joseph J.; Livraghi, Luca; Heryanto, Christa; McMillan, W. Owen; Jiggins, Chris D.; Gilbert, Lawrence E.; Martin, Arnaud; Oliver, ed., B. (January 2022, G3 Genes|Genomes|Genetics)

   Abstract As the genetic basis of natural and domesticated variation has been described in recent years, a number of hotspot genes have been repeatedly identified as the targets of selection, Heliconius butterflies display a spectacular diversity of pattern variants in the wild and the genetic basis of these patterns has been well-described. Here, we sought to identify the mechanism behind an unusual pattern variant that is instead found in captivity, the ivory mutant, in which all scales on both the wings and body become white or yellow. Using a combination of autozygosity mapping and coverage analysis from 37 captive individuals, we identify a 78-kb deletion at the cortex wing patterning locus, a gene which has been associated with wing pattern evolution in H. melpomene and 10 divergent lepidopteran species. This deletion is undetected among 458 wild Heliconius genomes samples, and its dosage explains both homozygous and heterozygous ivory phenotypes found in captivity. The deletion spans a large 5′ region of the cortex gene that includes a facultative 5′UTR exon detected in larval wing disk transcriptomes. CRISPR mutagenesis of this exon replicates the wing phenotypes from coding knock-outs of cortex, consistent with a functional role of ivory-deleted elements in establishing scale color fate. Population demographics reveal that the stock giving rise to the ivory mutant has a mixed origin from across the wild range of H. melpomene, and supports a scenario where the ivory mutation occurred after the introduction of cortex haplotypes from Ecuador. Homozygotes for the ivory deletion are inviable while heterozygotes are the targets of artificial selection, joining 40 other examples of allelic variants that provide heterozygous advantage in animal populations under artificial selection by fanciers and breeders. Finally, our results highlight the promise of autozygosity and association mapping for identifying the genetic basis of aberrant mutations in captive insect populations. 

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5. Transient use of hemolymph for hydraulic wing expansion in cicadas

   https://doi.org/10.1038/s41598-023-32533-4  

   Salcedo, Mary K.; Ellis, Tyler E.; Sáenz, Ángela S.; Lu, Joyce; Worrell, Terrell; Madigan, Michael L.; Socha, John J. (December 2023, Scientific Reports)

   Abstract Insect wings must be flexible, light, and strong to allow dynamic behaviors such as flying, mating, and feeding. When winged insects eclose into adults, their wings unfold, actuated hydraulically by hemolymph. Flowing hemolymph in the wing is necessary for functioning and healthy wings, both as the wing forms and as an adult. Because this process recruits the circulatory system, we asked, how much hemolymph is pumped into wings, and what happens to the hemolymph afterwards? Using Brood X cicadas ( Magicicada septendecim ), we collected 200 cicada nymphs, observing wing transformation over 2 h. Using dissection, weighing, and imaging of wings at set time intervals, we found that within 40 min after emergence, wing pads morphed into adult wings and total wing mass increased to ~ 16% of body mass. Thus, a significant amount of hemolymph is diverted from body to wings to effectuate expansion. After full expansion, in the ~ 80 min after, the mass of the wings decreased precipitously. In fact, the final adult wing is lighter than the initial folded wing pad, a surprising result. These results demonstrate that cicadas not only pump hemolymph into the wings, they then pump it out, producing a strong yet lightweight wing. 

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