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.1Kronfeld-Schor N. Dayan T. Partitioning of time as an ecological resource.Annu. Rev. Ecol. Evol. Syst. 2003; 34: 153-181Crossref Scopus (663) Google Scholar,2Penteriani V. del Mar Delgado M. Alonso-Alvarez C. Sergio F. The importance of visual cues for nocturnal species: eagle owls signal by badge brightness.Behav. Ecol. 2007; 18: 143-147Crossref Scopus (63) Google Scholar,3Schmitz L. Motani R. Morphological differences between the eyeballs of nocturnal and diurnal amniotes revisited from optical perspectives of visual environments.Vision Res. 2010; 50: 936-946Crossref PubMed Scopus (54) Google Scholar,4Barton R.A. Purvis A. Harvey P.H. Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores.Philos. Trans. R. Soc. Lond. B Biol. Sci. 1995; 348: 381-392Crossref PubMed Google Scholar,5Gerkema M.P. Davies W.I.L. Foster R.G. Menaker M. Hut R.A. The nocturnal bottleneck and the evolution of activity patterns in mammals.Proc. Biol. Sci. 2013; 280: 20130508Crossref PubMed Scopus (165) Google Scholar Although shifts in diel activity patterns have occurred numerous times over the course of vertebrate evolution,6Cox D.T.C. Gardner A.S. Gaston K.J. Diel niche variation in mammals associated with expanded trait space.Nat. Commun. 2021; 12: 1753Crossref PubMed Scopus (18) Google Scholar 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,7Mallarino R. Pillay N. Hoekstra H.E. Schradin C. African striped mice.Curr. Biol. 2018; 28: R299-R301Abstract Full Text Full Text PDF PubMed Scopus (10) Google Scholar,8Schumann D.M. Cooper H.M. Hofmeyr M.D. Bennett N.C. Circadian rhythm of locomotor activity in the four-striped field mouse, Rhabdomys pumilio: a diurnal African rodent.Physiol. Behav. 2005; 85: 231-239Crossref PubMed Scopus (34) Google Scholar,9Allen A.E. Mouland J.W. Rodgers J. Baño-Otálora B. Douglas R.H. Jeffery G. Vugler A.A. Brown T.M. Lucas R.J. Spectral sensitivity of cone vision in the diurnal murid Rhabdomys pumilio.J. Exp. Biol. 2020; 223https://doi.org/10.1242/jeb.215368Crossref Scopus (4) Google Scholar,10van der Merwe I. Lukáts Á. Bláhová V. Oosthuizen M.K. Bennett N.C. Němec P. The topography of rods, cones and intrinsically photosensitive retinal ganglion cells in the retinas of a nocturnal (Micaelamys namaquensis) and a diurnal (Rhabdomys pumilio) rodent.PLoS One. 2018; 13: e0202106Crossref PubMed Scopus (14) Google Scholar,11Bano-Otalora B. Moye M.J. Brown T. Lucas R.J. Diekman C.O. Belle M.D. Daily electrical activity in the master circadian clock of a diurnal mammal.eLife. 2021; 10: e68179https://doi.org/10.7554/eLife.68179Crossref PubMed Scopus (11) Google Scholar 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.