Exploring the role of gut microbiota in host feeding behavior among breeds in swine

Abstract

Background: The interplay between the gut microbiota and feeding behavior has consequences for host metabolism and health. The present study aimed to explore gut microbiota overall influence on feeding behavior traits and to identify specific microbes associated with the traits in three commercial swine breeds at three growth stages. Feeding behavior measures were obtained from 651 pigs of three breeds (Duroc, Landrace, and Large White) from an average 73 to 163 days of age. Seven feeding behavior traits covered the information of feed intake, feeder occupation time, feeding rate, and the number of visits to the feeder. Rectal swabs were collected from each pig at 73 ± 3, 123 ± 4, and 158 ± 4 days of age. DNA was extracted and subjected to 16 S rRNA gene sequencing.

Results: Differences in feeding behavior traits among breeds during each period were found. The proportion of phenotypic variances of feeding behavior explained by the gut microbial composition was small to moderate (ranged from 0.09 to 0.31). A total of 21, 10, and 35 amplicon sequence variants were found to be significantly (q-value < 0.05) associated with feeding behavior traits for Duroc, Landrace, and Large White across the three sampling time points. The identified amplicon sequence variants were annotated to five phyla, with Firmicutes being the most abundant. Those amplicon sequence variants were assigned to 28 genera, mainly including Christensenellaceae_R-7_group, Ruminococcaceae_UCG-004, Dorea, Ruminococcaceae_UCG-014, and Marvinbryantia.

Conclusions: This study demonstrated the importance of the gut microbial composition in interacting with the host feeding behavior and identified multiple archaea and bacteria associated with feeding behavior measures in pigs from either Duroc, Landrace, or Large White breeds at three growth stages. Our study provides insight into the interaction between gut microbiota and feeding behavior and highlights the genetic background and age effects in swine microbial studies.

Keywords: Breed; Feeding behavior; Growth stage; Gut microbiota; Swine.

Fig. 1

Spearman’s correlations of feeding behavior traits by breed during three periods. Correlations with P-value ≤ 0.001, ≤ 0.05, and > 0.05 are depicted in purple, pink, and grey, respectively. ADFI = average daily amount of feed consumed (g); AOTD = average daily feeder occupation time (s); ADFR = average daily feeding rate (g/min); ANVD = average daily number of visits to feeder; AFIV = average amount of feed consumed per visit (g); AOTV = average feeder occupation time per visit (s); AFRV = average feeding rate per visit (g/min). (A) Correlations of traits during P1; (B) Correlations of traits during P2; (C) Correlations of traits during P3

Fig. 2

Contrasts of feeding behavior traits among breeds during three periods. Data are presented as least squares mean with the confidence interval. Different letters a, b, and c denote P < 0.05 between breeds within each time point. Colors represent three breeds: Duroc (DR), Landrace (LR), and Large White (LW). The x-axis represents three periods: P1, P2, and P3. To avoid the overlaps, dots representing three breeds are depicted horizontally away from each other for each period. (A) AOTD = average daily feeder occupation time (s); (B) ADFR = average daily feeding rate (g/min); (C) ANVD = average daily number of visits to feeder; (D) AFIV = average amount of feed consumed per visit (g); (E) AOTV = average feeder occupation time per visit (s); (F) AFRV = average feeding rate per visit (g/min)

Fig. 3

Estimated microbiability (m²) for feeding behavior traits by breed and time points. Data are presented as mean with SE error bars. Colors represent three breeds: Duroc (DR), Landrace (LR), and Large White (LW). ADFI = average daily amount of feed consumed (g); AOTD = average feeder daily occupation time (s); ADFR = average daily feeding rate (g/min); ANVD = average daily number of visits to feeder; AFIV = average amount of feed consumed per visit (g); AOTV = average feeder occupation time per visit (s); AFRV = average feeding rate per visit (g/min). (A) The microbiability values at 73 days (T1); (B) The microbiability values at 123 days (T2); (C) The microbiability values at 158 days (T3)

Fig. 4

Taxonomy of ASVs significantly associated with feeding behavior traits by breed at each time point. Taxonomy is depicted at the combination of genus and phylum level. The x-axis represents three breeds: Duroc (DR), Landrace (LR), and Large White (LW). The y-axis represents the number of identified ASVs for each category. Colors from the same color scheme represent different genus levels from the same phylum

Fig. 5

Venn diagram of common and unique ASVs significantly associated with feeding behavior traits. (A) Across breed groups at each time point; (B) Across time points within each breed group

Fig. 6

The coefficient estimates of identified ASVs (FDR < 0.05) by breed at three time points. Scaled data are presented to make a comparison on a similar scale. Each ASV is referred by taxonomy (phylum, family, genus) and ASV number in the table corresponding to the plot on the right. (A) Combined results for Duroc (DR), Landrace (LR), and Large White (LW) at 73 days (T1); (B) Combined results for Duroc (DR), Landrace (LR), and Large White (LW) at 123 days (T2); (C) Results for Duroc (DR), Landrace (LR), and Large White (LW) at 158 days (T3)