TY - JOUR
T1 - The genomic basis of temporal niche evolution in a diurnal rodent
AU - Richardson, Rose
AU - Feigin, Charles Y.
AU - Bano-Otalora, Beatriz
AU - Johnson, Matthew R.
AU - Allen, Annette E.
AU - Park, Jongbeom
AU - McDowell, Richard J.
AU - Mereby, Sarah A.
AU - Lin, I. Hsuan
AU - Lucas, Robert J.
AU - Mallarino, Ricardo
N1 - Publisher Copyright:
© 2023 Elsevier Inc.
PY - 2023/8/7
Y1 - 2023/8/7
N2 - 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.1,2,3,4,5 Although shifts in diel activity patterns have occurred numerous times over the course of vertebrate evolution,6 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,7,8,9,10,11 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.
AB - 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.1,2,3,4,5 Although shifts in diel activity patterns have occurred numerous times over the course of vertebrate evolution,6 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,7,8,9,10,11 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.
KW - African striped mouse
KW - Rhabdomys
KW - circadian organization
KW - circadian rhythm
KW - comparative genomics
KW - diurnality
KW - molecular oscillator
KW - phototransduction
KW - temporal niche
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U2 - 10.1016/j.cub.2023.06.068
DO - 10.1016/j.cub.2023.06.068
M3 - Article
C2 - 37480852
AN - SCOPUS:85167479983
SN - 0960-9822
VL - 33
SP - 3289-3298.e6
JO - Current Biology
JF - Current Biology
IS - 15
ER -