Abstract
BackgroundNocturnally active gymnotiform weakly electric fish generate electric signals for communication and navigation, which can be energetically taxing. These fish mainly inhabit the Amazon basin, where some species prefer well-oxygenated waters and others live in oxygen-poor, stagnant habitats. The latter species show morphological, physiological, and behavioral adaptations for hypoxia-tolerance. However, there have been no studies of hypoxia tolerance on the molecular level. Globins are classic respiratory proteins. They function principally in oxygen-binding and -delivery in various tissues and organs. Here, we investigate the molecular evolution of alpha and beta hemoglobins, myoglobin, and neuroglobin in 12 gymnotiforms compared with other teleost fish.ResultsThe present study identified positively selected sites (PSS) on hemoglobin (Hb) and myoglobin (Mb) genes using different maximum likelihood (ML) methods; some PSS fall in structurally important protein regions. This evidence for the positive selection of globin genes suggests that the adaptive evolution of these genes has helped to enhance the capacity for oxygen storage and transport. Interestingly, a substitution of a Cys at a key site in the obligate air-breathing electric eel (Electrophorus electricus) is predicted to enhance oxygen storage of Mb and contribute to NO delivery during hypoxia. A parallel Cys substitution was also noted in an air-breathing African electric fish (Gymnarchus niloticus). Moreover, the expected pattern under normoxic conditions of high expression of myoglobin in heart and neuroglobin in the brain in two hypoxia-tolerant species suggests that the main effect of selection on these globin genes is on their sequence rather than their basal expression patterns.ConclusionResults indicate a clear signature of positive selection in the globin genes of most hypoxia-tolerant gymnotiform fishes, which are obligate or facultative air breathers. These findings highlight the critical role of globin genes in hypoxia tolerance evolution of Gymnotiform electric fishes.
Highlights
Active gymnotiform weakly electric fish generate electric signals for communication and navigation, which can be energetically taxing
The phylogenetic tree placed Gymnotiformes and Siluriformes together, and they had a closer relationship with Characiformes than Cypriniformes in the Mb gene tree
The topology based on the genes still failed to resolve the relationships within Gymnotiformes, which is not surprising since this has been difficult to resolve even with large datasets
Summary
Active gymnotiform weakly electric fish generate electric signals for communication and navigation, which can be energetically taxing. These fish mainly inhabit the Amazon basin, where some species prefer well-oxygenated waters and others live in oxygen-poor, stagnant habitats. The latter species show morphological, physiological, and behavioral adaptations for hypoxia-tolerance. They function principally in oxygenbinding and -delivery in various tissues and organs. Electrocytes are large cells capable of generating large ionic currents, especially sodium. Physiological studies show that performance-related costs of EOD generation may be surprisingly high, from 10 up to 30% of routine oxygen consumption [5]. The O2 consumption of gymnotiforms does not differ from that of other sized teleosts [6] suggesting that gymnotiforms have adaptations for energy efficiency
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