Sensory Rewiring in an Echolocator: Genome-Wide Modification of Retinogenic and Auditory Genes in the Bat Myotis davidii
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Sensory Rewiring in an Echolocator : Genome-Wide Modification of Retinogenic and Auditory Genes in the Bat Myotis davidii. / Hudson, Nicholas J.; Baker, Michelle L.; Hart, Nathan S.; Wynne, James W.; Gu, Quan; Huang, Zhiyong; Zhang, Guojie; Ingham, Aaron B.; Wang, Linfa; Reverter, Antonio.
I: G3: Genes, Genomes, Genetics, Bind 4, Nr. 10, 2014, s. 1825-1835.Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › fagfællebedømt
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TY - JOUR
T1 - Sensory Rewiring in an Echolocator
T2 - Genome-Wide Modification of Retinogenic and Auditory Genes in the Bat Myotis davidii
AU - Hudson, Nicholas J.
AU - Baker, Michelle L.
AU - Hart, Nathan S.
AU - Wynne, James W.
AU - Gu, Quan
AU - Huang, Zhiyong
AU - Zhang, Guojie
AU - Ingham, Aaron B.
AU - Wang, Linfa
AU - Reverter, Antonio
PY - 2014
Y1 - 2014
N2 - Bats comprise 20% of all mammalian species and display a number of characteristics, including true flight, echolocation, and a heightened ability to resist viral load that uniquely position this group for comparative genomic studies. Here we searched for evidence of genomic variation consistent with sensory rewiring through bat evolution. We focused on two species with divergent sensory preferences. Myotis davidii is a bat species that echolocates and possesses dim- but not daylight-adapted vision whereas the black flying fox (Pteropus alecto) has highly developed day vision but does not echolocate. Using the naked mole rat as a reference, we found five functional genes (CYP1A2, RBP3, GUCY2F, CRYBB1, and GRK7) encoding visual proteins that have degenerated into pseudogenes in M. davidii but not P. alecto. In a second approach genome-wide codon usage bias (CUB) was compared between the two bat species. This CUB ranking systematically enriched for vision-related (CLN8, RD3, IKZF1, LAMC3, CRX, SOX8, VAX2, HPS1, RHO, PRPH2 and SOX9) and hearing-related (TPRN, TMIE, SLC52A3, OTOF, WFS1, SOD1, TBX18, MAP1A, OTOS, GPX1 and USH1G) machinery in M. davidii but not P. alecto. All vision and hearing genes selectively enriched in M. davidii for which orthologs could be identified also were more biased in the echolocating M. lucifugus than the nonecholocating P. vampyrus. We suggest that the existence of codon bias in vision- and hearing-related genes in a species that has evolved echolocation implies CUB is part of evolution's toolkit to rewire sensory systems. We propose that the two genetic changes (pseudogene formation and CUB) collectively paint a picture of that incorporates a combination of destruction and gain-of-function. Together, they help explain how natural selection has reduced physiological costs associated with the development of a smaller eye poorly adapted to day vision but that also contribute to enhanced dim light vision and the hearing adaptations consonant with echolocation.
AB - Bats comprise 20% of all mammalian species and display a number of characteristics, including true flight, echolocation, and a heightened ability to resist viral load that uniquely position this group for comparative genomic studies. Here we searched for evidence of genomic variation consistent with sensory rewiring through bat evolution. We focused on two species with divergent sensory preferences. Myotis davidii is a bat species that echolocates and possesses dim- but not daylight-adapted vision whereas the black flying fox (Pteropus alecto) has highly developed day vision but does not echolocate. Using the naked mole rat as a reference, we found five functional genes (CYP1A2, RBP3, GUCY2F, CRYBB1, and GRK7) encoding visual proteins that have degenerated into pseudogenes in M. davidii but not P. alecto. In a second approach genome-wide codon usage bias (CUB) was compared between the two bat species. This CUB ranking systematically enriched for vision-related (CLN8, RD3, IKZF1, LAMC3, CRX, SOX8, VAX2, HPS1, RHO, PRPH2 and SOX9) and hearing-related (TPRN, TMIE, SLC52A3, OTOF, WFS1, SOD1, TBX18, MAP1A, OTOS, GPX1 and USH1G) machinery in M. davidii but not P. alecto. All vision and hearing genes selectively enriched in M. davidii for which orthologs could be identified also were more biased in the echolocating M. lucifugus than the nonecholocating P. vampyrus. We suggest that the existence of codon bias in vision- and hearing-related genes in a species that has evolved echolocation implies CUB is part of evolution's toolkit to rewire sensory systems. We propose that the two genetic changes (pseudogene formation and CUB) collectively paint a picture of that incorporates a combination of destruction and gain-of-function. Together, they help explain how natural selection has reduced physiological costs associated with the development of a smaller eye poorly adapted to day vision but that also contribute to enhanced dim light vision and the hearing adaptations consonant with echolocation.
KW - Bat
KW - Codon usage bias
KW - Evolution
KW - Pseudogene
KW - Vision
U2 - 10.1534/g3.114.011262
DO - 10.1534/g3.114.011262
M3 - Journal article
C2 - 25096539
AN - SCOPUS:84908457349
VL - 4
SP - 1825
EP - 1835
JO - G3: Genes, Genomes, Genetics (Bethesda)
JF - G3: Genes, Genomes, Genetics (Bethesda)
SN - 2160-1836
IS - 10
ER -
ID: 258276451