The little skate genome and the evolutionary emergence of wing-like fins

Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments 1 , 2 . However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the li...

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Veröffentlicht in:Nature (London) 2023-04, Vol.616 (7957), p.495-503
Hauptverfasser: Marlétaz, Ferdinand, de la Calle-Mustienes, Elisa, Acemel, Rafael D., Paliou, Christina, Naranjo, Silvia, Martínez-García, Pedro Manuel, Cases, Ildefonso, Sleight, Victoria A., Hirschberger, Christine, Marcet-Houben, Marina, Navon, Dina, Andrescavage, Ali, Skvortsova, Ksenia, Duckett, Paul Edward, González-Rajal, Álvaro, Bogdanovic, Ozren, Gibcus, Johan H., Yang, Liyan, Gallardo-Fuentes, Lourdes, Sospedra, Ismael, Lopez-Rios, Javier, Darbellay, Fabrice, Visel, Axel, Dekker, Job, Shubin, Neil, Gabaldón, Toni, Nakamura, Tetsuya, Tena, Juan J., Lupiáñez, Darío G., Rokhsar, Daniel S., Gómez-Skarmeta, José Luis
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container_end_page 503
container_issue 7957
container_start_page 495
container_title Nature (London)
container_volume 616
creator Marlétaz, Ferdinand
de la Calle-Mustienes, Elisa
Acemel, Rafael D.
Paliou, Christina
Naranjo, Silvia
Martínez-García, Pedro Manuel
Cases, Ildefonso
Sleight, Victoria A.
Hirschberger, Christine
Marcet-Houben, Marina
Navon, Dina
Andrescavage, Ali
Skvortsova, Ksenia
Duckett, Paul Edward
González-Rajal, Álvaro
Bogdanovic, Ozren
Gibcus, Johan H.
Yang, Liyan
Gallardo-Fuentes, Lourdes
Sospedra, Ismael
Lopez-Rios, Javier
Darbellay, Fabrice
Visel, Axel
Dekker, Job
Shubin, Neil
Gabaldón, Toni
Nakamura, Tetsuya
Tena, Juan J.
Lupiáñez, Darío G.
Rokhsar, Daniel S.
Gómez-Skarmeta, José Luis
description Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments 1 , 2 . However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins—including gene expression, chromatin occupancy and three-dimensional conformation—we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait. Skate-specific changes in the epigenome and its three-dimensional organization contributed to the evolution of the batoid fin morphology.
doi_str_mv 10.1038/s41586-023-05868-1
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We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait. 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However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins—including gene expression, chromatin occupancy and three-dimensional conformation—we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait. 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little skate genome and the evolutionary emergence of wing-like fins</title><author>Marlétaz, Ferdinand ; de la Calle-Mustienes, Elisa ; Acemel, Rafael D. ; Paliou, Christina ; Naranjo, Silvia ; Martínez-García, Pedro Manuel ; Cases, Ildefonso ; Sleight, Victoria A. ; Hirschberger, Christine ; Marcet-Houben, Marina ; Navon, Dina ; Andrescavage, Ali ; Skvortsova, Ksenia ; Duckett, Paul Edward ; González-Rajal, Álvaro ; Bogdanovic, Ozren ; Gibcus, Johan H. ; Yang, Liyan ; Gallardo-Fuentes, Lourdes ; Sospedra, Ismael ; Lopez-Rios, Javier ; Darbellay, Fabrice ; Visel, Axel ; Dekker, Job ; Shubin, Neil ; Gabaldón, Toni ; Nakamura, Tetsuya ; Tena, Juan J. ; Lupiáñez, Darío G. ; Rokhsar, Daniel S. ; Gómez-Skarmeta, José Luis</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c546t-6587cb42098fd82ee1c3a3a6bd4f6d5e40e6687c6796ce5f9f8dec4f21a804c63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>45/22</topic><topic>45/23</topic><topic>45/91</topic><topic>631/136/2086</topic><topic>631/181/2474</topic><topic>631/181/2806</topic><topic>631/208/212/2304</topic><topic>Animal Fins - anatomy &amp; histology</topic><topic>Animals</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Benthic environment</topic><topic>Biological Evolution</topic><topic>Chromatin</topic><topic>Chromosomes</topic><topic>Conformation</topic><topic>Embryogenesis</topic><topic>Evolution</topic><topic>Evolutionary developmental biology</topic><topic>Evolutionary genetics</topic><topic>Fins</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genes, Reporter - genetics</topic><topic>Genome</topic><topic>Genome evolution</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Homeodomain Proteins - genetics</topic><topic>Homeodomain Proteins - metabolism</topic><topic>HOX gene</topic><topic>Humanities and Social Sciences</topic><topic>Morphology</topic><topic>multidisciplinary</topic><topic>Nucleotide sequence</topic><topic>Phenotypes</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Signal transduction</topic><topic>Skates, Fish - anatomy &amp; histology</topic><topic>Skates, Fish - genetics</topic><topic>Vertebrates</topic><topic>Zebrafish</topic><topic>Zebrafish - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Marlétaz, Ferdinand</creatorcontrib><creatorcontrib>de la Calle-Mustienes, Elisa</creatorcontrib><creatorcontrib>Acemel, Rafael D.</creatorcontrib><creatorcontrib>Paliou, Christina</creatorcontrib><creatorcontrib>Naranjo, Silvia</creatorcontrib><creatorcontrib>Martínez-García, Pedro Manuel</creatorcontrib><creatorcontrib>Cases, Ildefonso</creatorcontrib><creatorcontrib>Sleight, Victoria A.</creatorcontrib><creatorcontrib>Hirschberger, Christine</creatorcontrib><creatorcontrib>Marcet-Houben, Marina</creatorcontrib><creatorcontrib>Navon, Dina</creatorcontrib><creatorcontrib>Andrescavage, Ali</creatorcontrib><creatorcontrib>Skvortsova, Ksenia</creatorcontrib><creatorcontrib>Duckett, Paul Edward</creatorcontrib><creatorcontrib>González-Rajal, Álvaro</creatorcontrib><creatorcontrib>Bogdanovic, Ozren</creatorcontrib><creatorcontrib>Gibcus, Johan H.</creatorcontrib><creatorcontrib>Yang, Liyan</creatorcontrib><creatorcontrib>Gallardo-Fuentes, Lourdes</creatorcontrib><creatorcontrib>Sospedra, Ismael</creatorcontrib><creatorcontrib>Lopez-Rios, Javier</creatorcontrib><creatorcontrib>Darbellay, Fabrice</creatorcontrib><creatorcontrib>Visel, Axel</creatorcontrib><creatorcontrib>Dekker, Job</creatorcontrib><creatorcontrib>Shubin, Neil</creatorcontrib><creatorcontrib>Gabaldón, Toni</creatorcontrib><creatorcontrib>Nakamura, Tetsuya</creatorcontrib><creatorcontrib>Tena, Juan J.</creatorcontrib><creatorcontrib>Lupiáñez, Darío G.</creatorcontrib><creatorcontrib>Rokhsar, Daniel S.</creatorcontrib><creatorcontrib>Gómez-Skarmeta, José Luis</creatorcontrib><creatorcontrib>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing &amp; Allied Health 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Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Marlétaz, Ferdinand</au><au>de la Calle-Mustienes, Elisa</au><au>Acemel, Rafael D.</au><au>Paliou, Christina</au><au>Naranjo, Silvia</au><au>Martínez-García, Pedro Manuel</au><au>Cases, Ildefonso</au><au>Sleight, Victoria A.</au><au>Hirschberger, Christine</au><au>Marcet-Houben, Marina</au><au>Navon, Dina</au><au>Andrescavage, Ali</au><au>Skvortsova, Ksenia</au><au>Duckett, Paul Edward</au><au>González-Rajal, Álvaro</au><au>Bogdanovic, Ozren</au><au>Gibcus, Johan H.</au><au>Yang, Liyan</au><au>Gallardo-Fuentes, Lourdes</au><au>Sospedra, Ismael</au><au>Lopez-Rios, Javier</au><au>Darbellay, Fabrice</au><au>Visel, Axel</au><au>Dekker, Job</au><au>Shubin, Neil</au><au>Gabaldón, Toni</au><au>Nakamura, Tetsuya</au><au>Tena, Juan J.</au><au>Lupiáñez, Darío G.</au><au>Rokhsar, Daniel S.</au><au>Gómez-Skarmeta, José Luis</au><aucorp>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The little skate genome and the evolutionary emergence of wing-like fins</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2023-04-20</date><risdate>2023</risdate><volume>616</volume><issue>7957</issue><spage>495</spage><epage>503</epage><pages>495-503</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><abstract>Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments 1 , 2 . However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins—including gene expression, chromatin occupancy and three-dimensional conformation—we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait. Skate-specific changes in the epigenome and its three-dimensional organization contributed to the evolution of the batoid fin morphology.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>37046085</pmid><doi>10.1038/s41586-023-05868-1</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0003-4120-0140</orcidid><orcidid>https://orcid.org/0000-0002-4130-7784</orcidid><orcidid>https://orcid.org/0000-0002-3165-036X</orcidid><orcidid>https://orcid.org/0000-0002-8704-2224</orcidid><orcidid>https://orcid.org/0000-0003-0019-1735</orcidid><orcidid>https://orcid.org/0000-0001-8124-4266</orcidid><orcidid>https://orcid.org/0000-0001-6942-3325</orcidid><orcidid>https://orcid.org/0000-0002-0851-7560</orcidid><orcidid>https://orcid.org/0000-0002-4529-3332</orcidid><orcidid>https://orcid.org/0000-0001-5631-0698</orcidid><orcidid>https://orcid.org/0000-0002-2119-2465</orcidid><orcidid>https://orcid.org/0000-0002-8784-5174</orcidid><orcidid>https://orcid.org/0000-0001-5680-0056</orcidid><orcidid>https://orcid.org/0000-0001-8165-7984</orcidid><orcidid>https://orcid.org/0000-0003-0183-1685</orcidid><orcidid>https://orcid.org/0000000181657984</orcidid><orcidid>https://orcid.org/0000000341200140</orcidid><orcidid>https://orcid.org/0000000287845174</orcidid><orcidid>https://orcid.org/0000000208517560</orcidid><orcidid>https://orcid.org/0000000156800056</orcidid><orcidid>https://orcid.org/0000000169423325</orcidid><orcidid>https://orcid.org/0000000221192465</orcidid><orcidid>https://orcid.org/0000000245293332</orcidid><orcidid>https://orcid.org/0000000241307784</orcidid><orcidid>https://orcid.org/000000023165036X</orcidid><orcidid>https://orcid.org/0000000300191735</orcidid><orcidid>https://orcid.org/0000000181244266</orcidid><orcidid>https://orcid.org/0000000156310698</orcidid><orcidid>https://orcid.org/0000000287042224</orcidid><orcidid>https://orcid.org/0000000301831685</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 0028-0836
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issn 0028-0836
1476-4687
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10115646
source MEDLINE; Springer Nature - Complete Springer Journals; Nature Journals Online
subjects 45/22
45/23
45/91
631/136/2086
631/181/2474
631/181/2806
631/208/212/2304
Animal Fins - anatomy & histology
Animals
BASIC BIOLOGICAL SCIENCES
Benthic environment
Biological Evolution
Chromatin
Chromosomes
Conformation
Embryogenesis
Evolution
Evolutionary developmental biology
Evolutionary genetics
Fins
Gene expression
Genes
Genes, Reporter - genetics
Genome
Genome evolution
Genomes
Genomics
Homeodomain Proteins - genetics
Homeodomain Proteins - metabolism
HOX gene
Humanities and Social Sciences
Morphology
multidisciplinary
Nucleotide sequence
Phenotypes
Science
Science (multidisciplinary)
Signal transduction
Skates, Fish - anatomy & histology
Skates, Fish - genetics
Vertebrates
Zebrafish
Zebrafish - genetics
title The little skate genome and the evolutionary emergence of wing-like fins
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