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1. Ultrabithorax Is a Micromanager of Hindwing Identity in Butterflies and Moths

   https://doi.org/10.3389/fevo.2021.643661  

   Tendolkar, Amruta ; Pomerantz, Aaron F. ; Heryanto, Christa ; Shirk, Paul D. ; Patel, Nipam H. ; Martin, Arnaud ( March 2021 , Frontiers in Ecology and Evolution)

   null (Ed.)

   The forewings and hindwings of butterflies and moths (Lepidoptera) are differentiated from each other, with segment-specific morphologies and color patterns that mediate a wide range of functions in flight, signaling, and protection. The Hox gene Ultrabithorax ( Ubx ) is a master selector gene that differentiates metathoracic from mesothoracic identities across winged insects, and previous work has shown this role extends to at least some of the color patterns from the butterfly hindwing. Here we used CRISPR targeted mutagenesis to generate Ubx loss-of-function somatic mutations in two nymphalid butterflies ( Junonia coenia , Vanessa cardui ) and a pyralid moth ( Plodia interpunctella ). The resulting mosaic clones yielded hindwing-to-forewing transformations, showing Ubx is necessary for specifying many aspects of hindwing-specific identities, including scale morphologies, color patterns, and wing venation and structure. These homeotic phenotypes showed cell-autonomous, sharp transitions between mutant and non-mutant scales, except for clones that encroached into the border ocelli (eyespots) and resulted in composite and non-autonomous effects on eyespot ring determination. In the pyralid moth, homeotic clones converted the folding and depigmented hindwing into rigid and pigmented composites, affected the wing-coupling frenulum, and induced ectopic scent-scales in male androconia. These data confirm Ubx is a master selector of lepidopteran hindwing identity and suggest it acts on many gene regulatory networks involved in wing development and patterning. 

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2. 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)

   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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3. 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)

   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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4. Phylogeography and population genetics reveal ring species patterns in a highly polymorphic California lily

   https://doi.org/10.1111/jbi.14313  

   Hernández, Adriana I. ; Landis, Jacob B. ; Specht, Chelsea D. ( January 2022 , Journal of Biogeography)

   Natural selection typically results in the homogenization of reproductive traits, reducing natural variation within populations; thus, highly polymorphic species present unresolved questions regarding the mechanisms that shape and maintain gene flow given a diversity of phenotypes. We used an integrative framework to characterize phenotypic diversity and assess how evolutionary history and population genetics affect the highly polymorphic nature of a California endemic lily.

   California, United States.

   Butterfly mariposa lily,Calochortus venustus(Liliaceae).

   We summarized phenotypic diversity at both metapopulation and subpopulation scales to explore spatial phenotypic distributions. We sampled 174 individuals across the species range representing multiple samples for each population and each phenotype. We used restriction‐site‐associated DNA sequencing (RAD‐Seq) to detect population clusters, gene flow between phenotypes and between populations, infer haplotype networks, and reconstruct ancestral range evolution to infer historical migration and range expansion.

   Polymorphic floral traits within the species such as petal pigmentation and distal spots are geographically structured, and inferred evolutionary history is consistent with a ring species pattern involving a complex of populations having experienced sequential change in genetic and phenotypic variation from the founding population. Populations remain interconnected yet have differentiated from each other along a bifurcating south‐to‐north range expansion, consequently indicating parallel evolution towards the white morphotype in the northern range. Thus, our phylogeographical analyses reveal morphological convergence with population genetic cohesion irrespective of phenotypic diversity.

   Phenotypic variation in the highly polymorphicCalochortus venustusis not due to genetic differentiation between phenotypes; rather there is genetic cohesion within six geographically defined populations, some of which maintain a high level of within‐population phenotypic diversity. Our results demonstrate that analyses of polymorphic taxa greatly benefit from disentangling phenotype from genotype at various spatial scales. We discuss results in light of ring species concepts and the need to determine the adaptive significance of the patterns we report.

    

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5. Incomplete reproductive isolation and low genetic differentiation despite floral divergence across varying geographic scales in Castilleja

   https://doi.org/10.1002/ajb2.1700  

   Wenzell, Katherine E. ; McDonnell, Angela J. ; Wickett, Norman J. ; Fant, Jeremie B. ; Skogen, Krissa A. ( July 2021 , American Journal of Botany)

   Divergence depends on the strength of selection and frequency of gene flow between taxa, while reproductive isolation relies on mating barriers and geographic distance. Less is known about how these processes interact at early stages of speciation. Here, we compared population‐level differentiation in floral phenotype and genetic sequence variation among recently divergedCastillejato explore patterns of diversification under different scenarios of reproductive isolation.

   Using target enrichment enabled by the Angiosperms353 probe set, we assessed genetic distance among 50 populations of fourCastillejaspecies. We investigated whether patterns of genetic divergence are explained by floral trait variation or geographic distance in two focal groups: the widespreadC. sessilifloraand the more restrictedC. purpureaspecies complex.

   We document thatC. sessilifloraand theC. purpureacomplex are characterized by high diversity in floral color across varying geographic scales. Despite phenotypic divergence, groups were not well supported in phylogenetic analyses, and little genetic differentiation was found across targeted Angiosperms353 loci. Nonetheless, a principal coordinate analysis of single nucleotide polymorphisms revealed differentiation withinC. sessilifloraacross floral morphs and geography and less differentiation among species of theC. purpureacomplex.

   Patterns of genetic distance inC. sessiliflorasuggest species cohesion maintained over long distances despite variation in floral traits. In theC. purpureacomplex, divergence in floral color across narrow geographic clines may be driven by recent selection on floral color. These contrasting patterns of floral and genetic differentiation reveal that divergence can arise via multiple eco‐evolutionary paths.

    

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