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Comprising more than 1,400 species, bats possess adaptations unique among mammals including powered flight, unexpected longevity, and extraordinary immunity. Some of the molecular mechanisms underlying these unique adaptations includes DNA repair, metabolism and immunity. However, analyses have been limited to a few divergent lineages, reducing the scope of inferences on gene family evolution across the Order Chiroptera. We conducted an exhaustive comparative genomic study of 37 bat species, one generated in this study, encompassing a large number of lineages, with a particular emphasis on multi-gene family evolution across immune and metabolic genes. In agreement with previous analyses, we found lineage-specific expansions of the APOBEC3 and MHC-I gene families, and loss of the proinflammatory PYHIN gene family. We inferred more than 1,000 gene losses unique to bats, including genes involved in the regulation of inflammasome pathways such as epithelial defence receptors, the natural killer gene complex and the interferon-gamma induced pathway. Gene set enrichment analyses revealed genes lost in bats are involved in defence response against pathogen-associated molecular patterns and damage-associated molecular patterns. Gene family evolution and selection analyses indicate bats have evolved fundamental functional differences compared to other mammals in both innate and adaptive immune system, with the potential to enhance antiviral immune response while dampening inflammatory signalling. In addition, metabolic genes have experienced repeated expansions related to convergent shifts to plant-based diets. Our analyses support the hypothesis that, in tandem with flight, ancestral bats had evolved a unique set of immune adaptations whose functional implications remain to be explored. 

Bats are famous for using their hearing to explore their environments, yet fewer people are aware that these flying mammals have both good night and daylight vision. Some bats can even see in color thanks to two light-sensitive proteins at the back of their eyes: S-opsin which detects blue and ultraviolet light and L-opsin which detects green and red light. Many species of bat, however, are missing one of these proteins and cannot distinguish any colors; in other words, they are completely color-blind. Some bat species found in Central and South America have independently lost their ability to see blue-ultraviolet light and have thus also lost their color vision. These bats have diverse diets – ranging from insects to fruits and even blood – and being able to distinguish color may offer an advantage in many of their activities, including hunting or foraging. The vision genes in these bats, therefore, give scientists an opportunity to explore how a seemingly important trait can be lost at the molecular level. Sadier, Davies et al. now report that S-opsin has been lost more than a dozen times during the evolutionary history of these Central and South American bats. The analysis used samples from 55 species, including animals caught from the wild and specimens from museums. As with other proteins, the instructions encoded in the gene sequence for S opsin need to be copied into a molecule of RNA before they can be translated into protein. As expected, S-opsin was lost several times because of changes in the gene sequence that disrupted the formation of the protein. However, at several points in these bats’ evolutionary history, additional changes have taken place that affected the production of the RNA or the protein, without an obvious change to the gene itself. This finding suggests that other studies that rely purely on DNA to understand evolution may underestimate how often traits may be lost. By capturing ‘evolution in action’, these results also provide a more complete picture of the molecular targets of evolution in a diverse set of bats.