Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies
Abstract Background Gene duplication events are critical for the evolution of new gene functions. Aristaless is a major regulator of distinct developmental processes. It is most known for its role during appendage development across animals. However, more recently other distinct biological functions...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-05-01
|
| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-023-01602-5 |
| _version_ | 1797827365076729856 |
|---|---|
| author | Erick X. Bayala Isabella Cisneros Darli Massardo Nicholas W. VanKuren Marcus R. Kronforst |
| author_facet | Erick X. Bayala Isabella Cisneros Darli Massardo Nicholas W. VanKuren Marcus R. Kronforst |
| author_sort | Erick X. Bayala |
| collection | DOAJ |
| description | Abstract Background Gene duplication events are critical for the evolution of new gene functions. Aristaless is a major regulator of distinct developmental processes. It is most known for its role during appendage development across animals. However, more recently other distinct biological functions have been described for this gene and its duplicates. Butterflies and moths have two copies of aristaless, aristaless1 (al1) and aristaless2 (al2), as a result of a gene duplication event. Previous work in Heliconius has shown that both copies appear to have novel functions related to wing color patterning. Here we expand our knowledge of the expression profiles associated with both ancestral and novel functions of Al1 across embryogenesis and wing pigmentation. Furthermore, we characterize Al2 expression, providing a comparative framework between gene copies within the same species, allowing us to understand the origin of new functions following gene duplication. Results Our work shows that the expression of both Al1 and Al2 is associated with the ancestral function of sensory appendage (leg, mouth, spines, and eyes) development in embryos. Interestingly, Al1 exhibits higher expression earlier in embryogenesis while the highest levels of Al2 expression are shifted to later stages of embryonic development. Furthermore, Al1 localization appears extranuclear while Al2 co-localizes tightly with nuclei earlier, and then also expands outside the nucleus later in development. Cellular expression of Al1 and Al2 in pupal wings is broadly consistent with patterns observed during embryogenesis. We also describe, for the first time, how Al1 localization appears to correlate with zones of anterior/posterior elongation of the body during embryonic growth, showcasing a possible new function related to Aristaless’ previously described role in appendage extension. Conclusions Overall, our data suggest that while both gene copies play a role in embryogenesis and wing pigmentation, the duplicates have diverged temporally and mechanistically across those functions. Our study helps clarify principles behind sub-functionalization and gene expression evolution associated with developmental functions following gene duplication events. |
| first_indexed | 2024-04-09T12:47:07Z |
| format | Article |
| id | doaj.art-3c0462633cea4833bec50e3fe2d1333e |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-09T12:47:07Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-3c0462633cea4833bec50e3fe2d1333e2023-05-14T11:27:47ZengBMCBMC Biology1741-70072023-05-0121111610.1186/s12915-023-01602-5Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterfliesErick X. Bayala0Isabella Cisneros1Darli Massardo2Nicholas W. VanKuren3Marcus R. Kronforst4Department of Ecology & Evolution, University of ChicagoDepartment of Ecology & Evolution, University of ChicagoDepartment of Ecology & Evolution, University of ChicagoDepartment of Ecology & Evolution, University of ChicagoDepartment of Ecology & Evolution, University of ChicagoAbstract Background Gene duplication events are critical for the evolution of new gene functions. Aristaless is a major regulator of distinct developmental processes. It is most known for its role during appendage development across animals. However, more recently other distinct biological functions have been described for this gene and its duplicates. Butterflies and moths have two copies of aristaless, aristaless1 (al1) and aristaless2 (al2), as a result of a gene duplication event. Previous work in Heliconius has shown that both copies appear to have novel functions related to wing color patterning. Here we expand our knowledge of the expression profiles associated with both ancestral and novel functions of Al1 across embryogenesis and wing pigmentation. Furthermore, we characterize Al2 expression, providing a comparative framework between gene copies within the same species, allowing us to understand the origin of new functions following gene duplication. Results Our work shows that the expression of both Al1 and Al2 is associated with the ancestral function of sensory appendage (leg, mouth, spines, and eyes) development in embryos. Interestingly, Al1 exhibits higher expression earlier in embryogenesis while the highest levels of Al2 expression are shifted to later stages of embryonic development. Furthermore, Al1 localization appears extranuclear while Al2 co-localizes tightly with nuclei earlier, and then also expands outside the nucleus later in development. Cellular expression of Al1 and Al2 in pupal wings is broadly consistent with patterns observed during embryogenesis. We also describe, for the first time, how Al1 localization appears to correlate with zones of anterior/posterior elongation of the body during embryonic growth, showcasing a possible new function related to Aristaless’ previously described role in appendage extension. Conclusions Overall, our data suggest that while both gene copies play a role in embryogenesis and wing pigmentation, the duplicates have diverged temporally and mechanistically across those functions. Our study helps clarify principles behind sub-functionalization and gene expression evolution associated with developmental functions following gene duplication events.https://doi.org/10.1186/s12915-023-01602-5HeliconiusAristalessAppendage formationGene duplicationSubfunctionalizationButterfly color patterning |
| spellingShingle | Erick X. Bayala Isabella Cisneros Darli Massardo Nicholas W. VanKuren Marcus R. Kronforst Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies BMC Biology Heliconius Aristaless Appendage formation Gene duplication Subfunctionalization Butterfly color patterning |
| title | Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies |
| title_full | Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies |
| title_fullStr | Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies |
| title_full_unstemmed | Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies |
| title_short | Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies |
| title_sort | divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies |
| topic | Heliconius Aristaless Appendage formation Gene duplication Subfunctionalization Butterfly color patterning |
| url | https://doi.org/10.1186/s12915-023-01602-5 |
| work_keys_str_mv | AT erickxbayala divergentexpressionofaristaless1andaristaless2duringembryonicappendageandpupalwingdevelopmentinbutterflies AT isabellacisneros divergentexpressionofaristaless1andaristaless2duringembryonicappendageandpupalwingdevelopmentinbutterflies AT darlimassardo divergentexpressionofaristaless1andaristaless2duringembryonicappendageandpupalwingdevelopmentinbutterflies AT nicholaswvankuren divergentexpressionofaristaless1andaristaless2duringembryonicappendageandpupalwingdevelopmentinbutterflies AT marcusrkronforst divergentexpressionofaristaless1andaristaless2duringembryonicappendageandpupalwingdevelopmentinbutterflies |