The genomic basis of temporal niche evolution in a diurnal rodent
Patterns of diel activity-how animals allocate their activity throughout the 24-h daily cycle-play key roles in shaping the internal physiology of an animal and its relationship with the external environment. Although shifts in diel activity patterns have occurred numerous times over the course of v...
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Veröffentlicht in: | Current biology 2023-08, Vol.33 (15), p.3289-3298.e6 |
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creator | Richardson, Rose Feigin, Charles Y Bano-Otalora, Beatriz Johnson, Matthew R Allen, Annette E Park, Jongbeom McDowell, Richard J Mereby, Sarah A Lin, I-Hsuan Lucas, Robert J Mallarino, Ricardo |
description | Patterns of diel activity-how animals allocate their activity throughout the 24-h daily cycle-play key roles in shaping the internal physiology of an animal and its relationship with the external environment.
Although shifts in diel activity patterns have occurred numerous times over the course of vertebrate evolution,
the genomic correlates of such transitions remain unknown. Here, we use the African striped mouse (Rhabdomys pumilio), a species that transitioned from the ancestrally nocturnal diel niche of its close relatives to a diurnal one,
to define patterns of naturally occurring molecular variation in diel niche traits. First, to facilitate genomic analyses, we generate a chromosome-level genome assembly of the striped mouse. Next, using transcriptomics, we show that the switch to daytime activity in this species is associated with a realignment of daily rhythms in peripheral tissues with respect to the light:dark cycle and the central circadian clock. To uncover selection pressures associated with this temporal niche shift, we perform comparative genomic analyses with closely related rodent species and find evidence of relaxation of purifying selection on striped mouse genes in the rod phototransduction pathway. In agreement with this, electroretinogram measurements demonstrate that striped mice have functional differences in dim-light visual responses compared with nocturnal rodents. Taken together, our results show that striped mice have undergone a drastic change in circadian organization and provide evidence that the visual system has been a major target of selection as this species transitioned to a novel temporal niche. |
doi_str_mv | 10.1016/j.cub.2023.06.068 |
format | Article |
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Although shifts in diel activity patterns have occurred numerous times over the course of vertebrate evolution,
the genomic correlates of such transitions remain unknown. Here, we use the African striped mouse (Rhabdomys pumilio), a species that transitioned from the ancestrally nocturnal diel niche of its close relatives to a diurnal one,
to define patterns of naturally occurring molecular variation in diel niche traits. First, to facilitate genomic analyses, we generate a chromosome-level genome assembly of the striped mouse. Next, using transcriptomics, we show that the switch to daytime activity in this species is associated with a realignment of daily rhythms in peripheral tissues with respect to the light:dark cycle and the central circadian clock. To uncover selection pressures associated with this temporal niche shift, we perform comparative genomic analyses with closely related rodent species and find evidence of relaxation of purifying selection on striped mouse genes in the rod phototransduction pathway. In agreement with this, electroretinogram measurements demonstrate that striped mice have functional differences in dim-light visual responses compared with nocturnal rodents. Taken together, our results show that striped mice have undergone a drastic change in circadian organization and provide evidence that the visual system has been a major target of selection as this species transitioned to a novel temporal niche.</description><identifier>ISSN: 0960-9822</identifier><identifier>ISSN: 1879-0445</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2023.06.068</identifier><identifier>PMID: 37480852</identifier><language>eng</language><publisher>England</publisher><subject>Animals ; Circadian Clocks ; Circadian Rhythm - genetics ; Genomics ; Mice ; Photoperiod ; Rodentia - genetics</subject><ispartof>Current biology, 2023-08, Vol.33 (15), p.3289-3298.e6</ispartof><rights>Copyright © 2023 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c400t-58ee04a2cfb77a9f0a1626137de55519e8cb6acca55d3a1547f9bd7399f164173</citedby><cites>FETCH-LOGICAL-c400t-58ee04a2cfb77a9f0a1626137de55519e8cb6acca55d3a1547f9bd7399f164173</cites><orcidid>0000-0002-8971-4864</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37480852$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Richardson, Rose</creatorcontrib><creatorcontrib>Feigin, Charles Y</creatorcontrib><creatorcontrib>Bano-Otalora, Beatriz</creatorcontrib><creatorcontrib>Johnson, Matthew R</creatorcontrib><creatorcontrib>Allen, Annette E</creatorcontrib><creatorcontrib>Park, Jongbeom</creatorcontrib><creatorcontrib>McDowell, Richard J</creatorcontrib><creatorcontrib>Mereby, Sarah A</creatorcontrib><creatorcontrib>Lin, I-Hsuan</creatorcontrib><creatorcontrib>Lucas, Robert J</creatorcontrib><creatorcontrib>Mallarino, Ricardo</creatorcontrib><title>The genomic basis of temporal niche evolution in a diurnal rodent</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>Patterns of diel activity-how animals allocate their activity throughout the 24-h daily cycle-play key roles in shaping the internal physiology of an animal and its relationship with the external environment.
Although shifts in diel activity patterns have occurred numerous times over the course of vertebrate evolution,
the genomic correlates of such transitions remain unknown. Here, we use the African striped mouse (Rhabdomys pumilio), a species that transitioned from the ancestrally nocturnal diel niche of its close relatives to a diurnal one,
to define patterns of naturally occurring molecular variation in diel niche traits. First, to facilitate genomic analyses, we generate a chromosome-level genome assembly of the striped mouse. Next, using transcriptomics, we show that the switch to daytime activity in this species is associated with a realignment of daily rhythms in peripheral tissues with respect to the light:dark cycle and the central circadian clock. To uncover selection pressures associated with this temporal niche shift, we perform comparative genomic analyses with closely related rodent species and find evidence of relaxation of purifying selection on striped mouse genes in the rod phototransduction pathway. In agreement with this, electroretinogram measurements demonstrate that striped mice have functional differences in dim-light visual responses compared with nocturnal rodents. Taken together, our results show that striped mice have undergone a drastic change in circadian organization and provide evidence that the visual system has been a major target of selection as this species transitioned to a novel temporal niche.</description><subject>Animals</subject><subject>Circadian Clocks</subject><subject>Circadian Rhythm - genetics</subject><subject>Genomics</subject><subject>Mice</subject><subject>Photoperiod</subject><subject>Rodentia - genetics</subject><issn>0960-9822</issn><issn>1879-0445</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUM9LwzAYDaK4Of0DvEiPXlq_pEmanGSIv2DgZZ5DmqZbRtvMph3435uxORQefIf3vvceD6FbDBkGzB82mRnLjADJM-AR4gxNsShkCpSyczQFySGVgpAJugphA4CJkPwSTfKCChCMTNF8ubbJyna-dSYpdXAh8XUy2Hbre90knTORtzvfjIPzXeK6RCeVG_sukr2vbDdco4taN8HeHO8Mfb48L5_e0sXH6_vTfJEaCjCkTFgLVBNTl0WhZQ0ac8JxXlSWMYalFabk2hjNWJVrzGhRy7IqcilrzCku8hl6PPhux7K1lYnRsaHa9q7V_bfy2qn_TOfWauV3CgMjUjARHe6PDr3_Gm0YVOuCsU2jO-vHoIigGAiVhEUpPkhN70PobX3KwaD226uNitur_fYKeMTe_u5vwdPH79j5D2xEgUU</recordid><startdate>20230807</startdate><enddate>20230807</enddate><creator>Richardson, Rose</creator><creator>Feigin, Charles Y</creator><creator>Bano-Otalora, Beatriz</creator><creator>Johnson, Matthew R</creator><creator>Allen, Annette E</creator><creator>Park, Jongbeom</creator><creator>McDowell, Richard J</creator><creator>Mereby, Sarah A</creator><creator>Lin, I-Hsuan</creator><creator>Lucas, Robert J</creator><creator>Mallarino, Ricardo</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8971-4864</orcidid></search><sort><creationdate>20230807</creationdate><title>The genomic basis of temporal niche evolution in a diurnal rodent</title><author>Richardson, Rose ; Feigin, Charles Y ; Bano-Otalora, Beatriz ; Johnson, Matthew R ; Allen, Annette E ; Park, Jongbeom ; McDowell, Richard J ; Mereby, Sarah A ; Lin, I-Hsuan ; Lucas, Robert J ; Mallarino, Ricardo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c400t-58ee04a2cfb77a9f0a1626137de55519e8cb6acca55d3a1547f9bd7399f164173</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Circadian Clocks</topic><topic>Circadian Rhythm - genetics</topic><topic>Genomics</topic><topic>Mice</topic><topic>Photoperiod</topic><topic>Rodentia - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Richardson, Rose</creatorcontrib><creatorcontrib>Feigin, Charles Y</creatorcontrib><creatorcontrib>Bano-Otalora, Beatriz</creatorcontrib><creatorcontrib>Johnson, Matthew R</creatorcontrib><creatorcontrib>Allen, Annette E</creatorcontrib><creatorcontrib>Park, Jongbeom</creatorcontrib><creatorcontrib>McDowell, Richard J</creatorcontrib><creatorcontrib>Mereby, Sarah A</creatorcontrib><creatorcontrib>Lin, I-Hsuan</creatorcontrib><creatorcontrib>Lucas, Robert J</creatorcontrib><creatorcontrib>Mallarino, Ricardo</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Richardson, Rose</au><au>Feigin, Charles Y</au><au>Bano-Otalora, Beatriz</au><au>Johnson, Matthew R</au><au>Allen, Annette E</au><au>Park, Jongbeom</au><au>McDowell, Richard J</au><au>Mereby, Sarah A</au><au>Lin, I-Hsuan</au><au>Lucas, Robert J</au><au>Mallarino, Ricardo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The genomic basis of temporal niche evolution in a diurnal rodent</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2023-08-07</date><risdate>2023</risdate><volume>33</volume><issue>15</issue><spage>3289</spage><epage>3298.e6</epage><pages>3289-3298.e6</pages><issn>0960-9822</issn><issn>1879-0445</issn><eissn>1879-0445</eissn><abstract>Patterns of diel activity-how animals allocate their activity throughout the 24-h daily cycle-play key roles in shaping the internal physiology of an animal and its relationship with the external environment.
Although shifts in diel activity patterns have occurred numerous times over the course of vertebrate evolution,
the genomic correlates of such transitions remain unknown. Here, we use the African striped mouse (Rhabdomys pumilio), a species that transitioned from the ancestrally nocturnal diel niche of its close relatives to a diurnal one,
to define patterns of naturally occurring molecular variation in diel niche traits. First, to facilitate genomic analyses, we generate a chromosome-level genome assembly of the striped mouse. Next, using transcriptomics, we show that the switch to daytime activity in this species is associated with a realignment of daily rhythms in peripheral tissues with respect to the light:dark cycle and the central circadian clock. To uncover selection pressures associated with this temporal niche shift, we perform comparative genomic analyses with closely related rodent species and find evidence of relaxation of purifying selection on striped mouse genes in the rod phototransduction pathway. In agreement with this, electroretinogram measurements demonstrate that striped mice have functional differences in dim-light visual responses compared with nocturnal rodents. Taken together, our results show that striped mice have undergone a drastic change in circadian organization and provide evidence that the visual system has been a major target of selection as this species transitioned to a novel temporal niche.</abstract><cop>England</cop><pmid>37480852</pmid><doi>10.1016/j.cub.2023.06.068</doi><orcidid>https://orcid.org/0000-0002-8971-4864</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Circadian Clocks Circadian Rhythm - genetics Genomics Mice Photoperiod Rodentia - genetics |
title | The genomic basis of temporal niche evolution in a diurnal rodent |
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