TY - JOUR

T1 - Adaptive genomic evolution of opsins reveals that early mammals flourished in nocturnal environments

AU - Borges, Rui

AU - Johnson, Warren E.

AU - O'Brien, Stephen J.

AU - Gomes, Cidalia

AU - Heesy, Christopher P.

AU - Antunes, Agostinho

PY - 2018/2/5

Y1 - 2018/2/5

N2 - Background: Based on evolutionary patterns of the vertebrate eye, Walls (1942) hypothesized that early placental mammals evolved primarily in nocturnal habitats. However, not only Eutheria, but all mammals show photic characteristics (i.e. dichromatic vision, rod-dominated retina) suggestive of a scotopic eye design.Results: Here, we used integrative comparative genomic and phylogenetic methodologies employing the photoreceptive opsin gene family in 154 mammals to test the likelihood of a nocturnal period in the emergence of all mammals. We showed that mammals possess genomic patterns concordant with a nocturnal ancestry. The loss of the RH2, VA, PARA, PARIE and OPN4x opsins in all mammals led us to advance a probable and most-parsimonious hypothesis of a global nocturnal bottleneck that explains the loss of these genes in the emerging lineage (> > 215.5 million years ago). In addition, ancestral character reconstruction analyses provided strong evidence that ancestral mammals possessed a nocturnal lifestyle, ultra-violet-sensitive vision, low visual acuity and low orbit convergence (i.e. panoramic vision).Conclusions: Overall, this study provides insight into the evolutionary history of the mammalian eye while discussing important ecological aspects of the photic paleo-environments ancestral mammals have occupied.

AB - Background: Based on evolutionary patterns of the vertebrate eye, Walls (1942) hypothesized that early placental mammals evolved primarily in nocturnal habitats. However, not only Eutheria, but all mammals show photic characteristics (i.e. dichromatic vision, rod-dominated retina) suggestive of a scotopic eye design.Results: Here, we used integrative comparative genomic and phylogenetic methodologies employing the photoreceptive opsin gene family in 154 mammals to test the likelihood of a nocturnal period in the emergence of all mammals. We showed that mammals possess genomic patterns concordant with a nocturnal ancestry. The loss of the RH2, VA, PARA, PARIE and OPN4x opsins in all mammals led us to advance a probable and most-parsimonious hypothesis of a global nocturnal bottleneck that explains the loss of these genes in the emerging lineage (> > 215.5 million years ago). In addition, ancestral character reconstruction analyses provided strong evidence that ancestral mammals possessed a nocturnal lifestyle, ultra-violet-sensitive vision, low visual acuity and low orbit convergence (i.e. panoramic vision).Conclusions: Overall, this study provides insight into the evolutionary history of the mammalian eye while discussing important ecological aspects of the photic paleo-environments ancestral mammals have occupied.

KW - Nocturnal bottleneck

KW - Mammals

KW - Opsins

KW - Nocturnal lifestyle

KW - Ultra

KW - violet sensitive vision

KW - Panoramic vision

KW - Visual acuity

KW - VERTEBRATE VISUAL PIGMENTS

KW - DIM-LIGHT-VISION

KW - MOLECULAR EVOLUTION

KW - ULTRAVIOLET VISION

KW - ORBIT ORIENTATION

KW - PRIMATES

KW - PHOTORECEPTORS

KW - ADAPTATION

KW - LIKELIHOOD

KW - ACCURACY

KW - Ultra-violet sensitive vision

KW - Opsins/chemistry

KW - Synteny

KW - Adaptation, Biological

KW - Selection, Genetic

KW - Mammals/genetics

KW - Biological Evolution

KW - Animals

KW - Environment

KW - Genome

KW - Evolution, Molecular

UR - http://www.scopus.com/inward/record.url?scp=85041400949&partnerID=8YFLogxK

U2 - 10.1186/s12864-017-4417-8

DO - 10.1186/s12864-017-4417-8

M3 - статья

C2 - 29402215

VL - 19

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 121

ER -