Adaptive Functional Diversification of Lysozyme in Insectivorous Bats

Abstract

The role of gene duplication in generating new genes and novel functions is well recognized and is exemplified by the digestion-related protein lysozyme. In ruminants, duplicated chicken-type lysozymes facilitate the degradation of symbiotic bacteria in the foregut. Chicken-type lysozyme has also been reported to show chitinase-like activity, yet no study has examined the molecular evolution of lysozymes in species that specialize on eating insects. Insectivorous bats number over 900 species, and lysozyme expression in the mouths of some of these species is associated with the ingestion of insect cuticle, suggesting a chitinase role. Here, we show that chicken-type lysozyme has undergone multiple duplication events in a major family of insect-eating bats (Vespertilionidae) and that new duplicates have undergone molecular adaptation. Examination of duplicates from two insectivorous bats-Pipistrellus abramus and Scotophilus kuhlii-indicated that the new copy was highly expressed in the tongue, whereas the other one was less tissue-specific. Functional assays applied to pipistrelle lysozymes confirmed that, of the two copies, the tongue duplicate was more efficient at breaking down glycol chitin, a chitin derivative. These results suggest that the evolution of lysozymes in vespertilionid bats has likely been driven in part by natural selection for insectivory.

Dietary Diversification and Specialization in Neotropical Bats Facilitated by Early Molecular Evolution

“…Strong candidates for molecular adaptation include NPC1L1 , implicated in lipid transport, with mutations linked to coronary heart disease and lipid storage disorder Niemann–Pick disease, and PGA3 , which encodes a precursor of the major digestive protease pepsin. To date, there are no published studies of adaptations relating purely to insectivory in phyllostomids; however, duplications and selection in the lysozyme C gene have been related to chitin catabolism in members of the insectivorous bat family Vespertilionidae ( Liu et al 2014 ). Our results may thus reflect specific adaptations to the relatively higher protein and fat content of animal-based diets.…”

Chitinase genes ( CHIA s) provide genomic footprints of a post-Cretaceous dietary radiation in placental mammals

“…S3), because this would seem to be a simple mechanism to increase chitinase activity when adapting to a chitin-rich diet. These chitinophagous, CHIA-limited mammals may be compensating via alternative mechanisms, such as increasing the expression of another CHIA or using chitin-digesting bacteria ( 30 , 31 ), chitinolytic lysozymes ( 32 ), or an additional mammalian chitinase, chitotriosidase (CHIT1) ( 33 ). CHIT1 is generally expressed in immunity-related tissues ( 33 , 34 ), but we found evidence that pangolin salivary glands express CHIT1 alongside CHIA5 (table S3), possibly suggesting co-option for digestive function.…”

Lineage‐specific duplication and adaptive evolution of bitter taste receptor genes in bats

“…However, our data from bats are not consistent with this claim, because only Myotis bats have more Tas2r genes than frugivorous and other insectivorous bats (Figure ). Despite the difference in dietary components, both Myotis and non‐ Myotis insectivorous bats appear to most commonly feed on insects from the orders Coleoptera (beetles), Lepidoptera (moths and butterflies) and Diptera (flies) (Hill & Smith, ; Liu et al., ). Thus, there is no clear‐cut correlation between diet and Tas2r gene number in bats.…”