Investigation of muscle transcriptomes using gradient boosting machine learning identifies molecular predictors of feed efficiency in growing pigs

BACKGROUND: Improving feed efficiency (FE) is a major challenge in pig production. This complex trait is characterized by a high variability. Therefore, the identification of predictors of FE may be a relevant strategy to reduce phenotyping efforts in breeding and selection programs. The aim of this study was to investigate the suitability of expressed muscle genes in prediction of FE traits in growing pigs. The approach considered different transcriptomics experiments to cover a large range of FE values and identify reliable predictors. RESULTS: Microarrays data were obtained from longissimus muscles of two lines divergently selected for residual feed intake (RFI). Pigs (n = 71) from three experiments belonged to generations 6 to 8 of selection, were fed either a diet with a standard composition or a diet rich in fiber and lipids, received feed ad libitum or at restricted level, and weighed between 80 and 115 kg at slaughter. For each pig, breeding value for RFI was estimated (RFI-BV), and feed conversion ratio (FCR) and energy-based feed conversion ratio (FCRe) were calculated during the test periods. Gradient boosting algorithms were used on the merged muscle transcriptomes to identify very important predictors of FE traits. About 20,405 annotated molecular probes were commonly expressed in longissimus muscle across experiments. Six to 267 expressed muscle genes covering a variety of biological processes were found as important predictors for RFI-BV (R(2) = 0.63–0.65), FCR (R(2) = 0.61–0.70) and FCRe (R(2) = 0.49–0.52). The error of prediction was less than 8% for FCR. Altogether, 56 predictors were common to RFI-BV and FCR. Expression levels of 24 target genes were further measured by qPCR. Linear regression confirmed the good accuracy of combining mRNA levels of these genes to fit FE traits (RFI-BV: R(2) = 0.73, FRC: R(2) = 0.76; FCRe: R(2) = 0.75). Stepwise regression procedure highlighted 10 genes (FKBP5, MUM1, AKAP12, FYN, TMED3, PHKB, TGF, SOCS6, ILR4, and FRAS1) in a linear combination predicting FCR and FCRe. In addition, FKBP5 and expression levels of five other genes (IGF2, SERINC3, CSRNP3, EZR and RPL16) significantly contributed to RFI-BV. CONCLUSION: It was possible to identify few genes expressed in muscle that might be reliable predictors of feed efficiency. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-6010-9) contains supplementary material, which is available to authorized users.