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This content will become publicly available on August 15, 2024

Title: Sex-linked gene traffic underlies the acquisition of sexually dimorphic UV color vision in Heliconius butterflies

The acquisition of novel sexually dimorphic traits poses an evolutionary puzzle: How do new traits arise and become sex-limited? Recently acquired color vision, sexually dimorphic in animals like primates and butterflies, presents a compelling model for understanding how traits become sex-biased. For example, someHeliconiusbutterflies uniquely possess UV (ultraviolet) color vision, which correlates with the expression of two differentially tuned UV-sensitive rhodopsins, UVRh1 and UVRh2. To discover how such traits become sexually dimorphic, we studiedHeliconius charithonia, which exhibits female-specific UVRh1 expression. We demonstrate that females, but not males, discriminate different UV wavelengths. Through whole-genome shotgun sequencing and assembly of theH. charithoniagenome, we discovered thatUVRh1is present on the W chromosome, making it obligately female-specific. By knocking outUVRh1, we show that UVRh1 protein expression is absent in mutant female eye tissue, as in wild-type male eyes. A PCR survey ofUVRh1sex-linkage across the genus shows that species with female-specific UVRh1 expression lackUVRh1gDNA in males. Thus, acquisition of sex linkage is sufficient to achieve female-specific expression ofUVRh1, though this does not preclude other mechanisms, likecis-regulatory evolution from also contributing. Moreover, both this event, and mutations leading to differential UV opsin sensitivity, occurred early in the history ofHeliconius. These results suggest a path for acquiring sexual dimorphism distinct from existing mechanistic models. We propose a model where gene traffic to heterosomes (the W or the Y) genetically partitions a trait by sex before a phenotype shifts (spectral tuning of UV sensitivity).

 
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Award ID(s):
1656260
NSF-PAR ID:
10507261
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences U.S.A.
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
120
Issue:
33
ISSN:
0027-8424
Subject(s) / Keyword(s):
["sex chromosome","genome assembly","butterfly","color vision","opsin"]
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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    Graphical Abstract 
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