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The molecular origins of dim-light vision in mammals

Reconstructed ancestral mammalian rhodopsins show altered function in the laboratory, indicative of adaptive evolution related to a nocturnal lifestyle. This is consistent with early theories and recent data suggesting nocturnality in ancient fossil lineages leading to mammals.

A longstanding theory postulates that mammals, one of the most successful groups of living land vertebrates, were nocturnal. This theory explains anatomical similarities between early fossil mammals and modern nocturnal mammals, and also provides an explanation for the evolution of a constant body temperature, which would have allowed early mammals to be more active during cooler nighttime conditions. However, finding corroboration of this hypothesis in the fossil record has been difficult. This study took an alternative approach, and used phylogenetic methods to trace the molecular evolution of rhodopsin, a visual pigment of the eye that is responsible for vision at night and under dim-light conditions, back to the origin of mammals in the Triassic. The hypothetical gene sequence of the first mammalian rhodopsin was computationally estimated and recreated in the laboratory, and then tested for function. The reconstructed mammal rhodopsin demonstrated a light absorption spectrum similar to many day-active/crepuscular mammals such as cows, but also displayed other features that are otherwise found only in nocturnal animals.

The researchers also applied molecular evolutionary analyses of selection to test for nocturnality. These methods can be used to calculate the extent of selection pressure acting on a gene or protein, for example during times of environmental change or major evolutionary radiations. The results showed that remarkable changes in rhodopsin must have occurred on the lineage leading to therian mammals, which originated roughly 70 million years after the first true mammals and include, among marsupial and placental species, modern humans. These observed changes are in accordance with recent fossil finds of early therians that witness a dramatic shift in the evolution and ecological diversity of mammals during the mid Mesozoic. The results emphasize the importance of cross-disciplinary collaborations in obtaining a comprehensive picture of the evolution of life.

This work was a collaboration between the HFSP-funded Chang lab, and Constanze Bickelmann and Johannes Müller, paleontologists at the Humboldt Museum in Berlin. The cross-disciplinary work developed from an HFSP-funded project with Massimo Olivucci (Siena, Italy) to investigate the evolution of quantum mechanical properties of ancestral pigments, and provides key paleontological insights into visual pigment evolution.

Reference

The molecular origin and evolution of dim-light vision in mammals. Bickelmann C, Morrow JM, Du J, Schott RK., van Hazel I, Lim S, Muller J, & Chang BSW. Evolution. 2015 69(11):2995-3003.

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