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 |
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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 |
format | Article |
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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.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-023-05868-1</identifier><identifier>PMID: 37046085</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>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</subject><ispartof>Nature (London), 2023-04, Vol.616 (7957), p.495-503</ispartof><rights>The Author(s) 2023</rights><rights>2023. The Author(s).</rights><rights>Copyright Nature Publishing Group Apr 20, 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c546t-6587cb42098fd82ee1c3a3a6bd4f6d5e40e6687c6796ce5f9f8dec4f21a804c63</citedby><cites>FETCH-LOGICAL-c546t-6587cb42098fd82ee1c3a3a6bd4f6d5e40e6687c6796ce5f9f8dec4f21a804c63</cites><orcidid>0000-0003-4120-0140 ; 0000-0002-4130-7784 ; 0000-0002-3165-036X ; 0000-0002-8704-2224 ; 0000-0003-0019-1735 ; 0000-0001-8124-4266 ; 0000-0001-6942-3325 ; 0000-0002-0851-7560 ; 0000-0002-4529-3332 ; 0000-0001-5631-0698 ; 0000-0002-2119-2465 ; 0000-0002-8784-5174 ; 0000-0001-5680-0056 ; 0000-0001-8165-7984 ; 0000-0003-0183-1685 ; 0000000181657984 ; 0000000341200140 ; 0000000287845174 ; 0000000208517560 ; 0000000156800056 ; 0000000169423325 ; 0000000221192465 ; 0000000245293332 ; 0000000241307784 ; 000000023165036X ; 0000000300191735 ; 0000000181244266 ; 0000000156310698 ; 0000000287042224 ; 0000000301831685</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41586-023-05868-1$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41586-023-05868-1$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,777,781,882,27905,27906,41469,42538,51300</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37046085$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/2229307$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><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><title>The little skate genome and the evolutionary emergence of wing-like fins</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><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.</description><subject>45/22</subject><subject>45/23</subject><subject>45/91</subject><subject>631/136/2086</subject><subject>631/181/2474</subject><subject>631/181/2806</subject><subject>631/208/212/2304</subject><subject>Animal Fins - anatomy & histology</subject><subject>Animals</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Benthic environment</subject><subject>Biological Evolution</subject><subject>Chromatin</subject><subject>Chromosomes</subject><subject>Conformation</subject><subject>Embryogenesis</subject><subject>Evolution</subject><subject>Evolutionary developmental biology</subject><subject>Evolutionary genetics</subject><subject>Fins</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genes, Reporter - genetics</subject><subject>Genome</subject><subject>Genome evolution</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Homeodomain Proteins - genetics</subject><subject>Homeodomain Proteins - metabolism</subject><subject>HOX gene</subject><subject>Humanities and Social Sciences</subject><subject>Morphology</subject><subject>multidisciplinary</subject><subject>Nucleotide sequence</subject><subject>Phenotypes</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Signal transduction</subject><subject>Skates, Fish - anatomy & histology</subject><subject>Skates, Fish - genetics</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><subject>Zebrafish - 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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 & 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 & 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 & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing & Allied Health 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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> |
fulltext | fulltext |
identifier | ISSN: 0028-0836 |
ispartof | Nature (London), 2023-04, Vol.616 (7957), p.495-503 |
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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