Dietary and flight energetic adaptations in a salivary gland transcriptome of an insectivorous bat.
We hypothesized that evolution of salivary gland secretory proteome has been important in adaptation to insectivory, the most common dietary strategy among Chiroptera. A submandibular salivary gland (SMG) transcriptome was sequenced for the little brown bat, Myotis lucifugus. The likely secretory proteome of 23 genes included seven (RETNLB, PSAP, CLU, APOE, LCN2, C3, CEL) related to M. lucifugus insectivorous diet and metabolism. Six of the secretory proteins probably are endocrine, whereas one (CEL) most likely is exocrine. The encoded proteins are associated with lipid hydrolysis, regulation of lipid metabolism, lipid transport, and insulin resistance. They are capable of processing exogenous lipids for flight metabolism while foraging. Salivary carboxyl ester lipase (CEL) is thought to hydrolyze insect lipophorins, which probably are absorbed across the gastric mucosa during feeding. The other six proteins are predicted either to maintain these lipids at high blood concentrations or to facilitate transport and uptake by flight muscles. Expression of these seven genes and coordinated secretion from a single organ is novel to this insectivorous bat, and apparently has evolved through instances of gene duplication, gene recruitment, and nucleotide selection. Four of the recruited genes are single-copy in the Myotis genome, whereas three have undergone duplication(s) with two of these genes exhibiting evolutionary 'bursts' of duplication resulting in multiple paralogs. Evidence for episodic directional selection was found for six of seven genes, reinforcing the conclusion that the recruited genes have important roles in adaptation to insectivory and the metabolic demands of flight. Intragenic frequencies of mobile- element-like sequences differed from frequencies in the whole M. lucifugus genome. Differences among recruited genes imply separate evolutionary trajectories and that adaptation was not a single, coordinated event.
Department of Biological Sciences, Texas Tech University, Lubbock, Texas, United States of America.
Carleton J
CJ
Phillips
Department of Biological Sciences, Texas Tech University, Lubbock, Texas, United States of America.
Caleb D
CD
Phillips
Department of Biology, Emory University, Atlanta, Georgia, United States of America ; Department of Math and Computer Science, Emory University, Atlanta, Georgia, United States of America.
Jeremy
J
Goecks
Departamento de Ecología y Evolución, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay.
Enrique P
EP
Lessa
Department of Biological Sciences, Texas Tech University, Lubbock, Texas, United States of America.
Cibele G
CG
Sotero-Caio
Department of Biological Sciences, School of Dental Medicine, Case Western Reserve University, Cleveland, Ohio, United States of America.
Bernard
B
Tandler
Department of Biology, Pennsylvania State University, Altoona College, Altoona, Pennsylvania, United States of America.
Michael R
MR
Gannon
Department of Biological Sciences, Texas Tech University, Lubbock, Texas, United States of America.
Robert J
RJ
Baker
D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D001692:Biological Transport; D002685:Chiroptera / Q000235:genetics* / Q000378:metabolism / Q000502:physiology; D004032:Diet; D004041:Dietary Fats / Q000378:metabolism; D004734:Energy Metabolism / Q000235:genetics*; D019143:Evolution, Molecular; D005426:Flight, Animal / Q000502:physiology*; D018628:Gene Dosage; D020440:Gene Duplication; D006868:Hydrolysis; D006949:Hyperlipidemias / Q000235:genetics; D050356:Lipid Metabolism / Q000235:genetics; D040901:Proteomics; D013363:Submandibular Gland / Q000378:metabolism*; D059467:Transcriptome
D004041:Dietary Fats