KISS1 Knockout Boars Have Decreased Concentrations of Gonadotropins Leading to Smaller Testes and Reduced Skatole in Backfat

Abstract In swine production, boars are castrated to prevent boar taint from testicular androgens and skatole accumulation in fat. Kisspeptin (KISS1) regulates secretion of gonadotropins and gonadal steroids. We used boars from our line of KISS1-/-pigs (10.3389/fgene.2022.1078991) to understand how loss of KISS1 function affects compounds causing boar taint. Boars were fed ad libitum during development. Body weights and testicular volume (TV) were collected at weaning, 40, 70, 100, 130, 160, and 190 d of age using TV = 4/3*π *a*b2*2 and subtracting scrotal skin thickness measured by a Harpenden skinfold caliper. Average daily gain (ADG) was calculated by subtracting the beginning from ending body weight at each age range and dividing by the number of days. At each age, a blood serum sample was collected by jugular venipuncture to quantify changes in hormones during development. Serum concentrations of luteinizing hormone (LH), follicle-stimulating hormone (FSH) and testosterone were quantified with radioimmunoassay and analyzed as repeated measures with genotype (KISS1+/+; KISS1+/-; KISS1-/-; n = 8 – 20 animals per genotype) and age as the fixed effects. Concentrations of androstenone and skatole in backfat (quantified using ELISA and HPLC, respectively) were log transformed and analyzed with ANOVA. Body weight did not differ among KISS1 genotypes but increased normally with age (P < 0.0001). During development, KISS1+/+ and KISS1+/- boars grew at similar rates. Although the ADG of KISS1-/-boars was similar to other genotypes up to 160 d of age, ADG was reduced at 190 d of age (age x genotype; P < 0.05). Mean concentrations of LH and FSH in KISS1+/+ and KISS1+/- boars were similar throughout development (LH, 1.16 ±0.11 and 1.34 ± 0.17 ng/mL; FSH, 0.88 ± 0.06 and 0.89 ± 0.05 ng/mL, respectively), and were greater than KISS1-/- boars (LH, 0.38 ± 0.23 ng/mL; FSH, 0.56 ± 0.07 ng/mL; P < 0.05). TV of KISS1+/+ and KISS1+/- boars did not differ during development and was greater than KISS1-/- boars (P < 0.05), for which testes could not be palpated after 100 d of age. Testosterone concentrations in KISS1+/+ and KISS1+/- increased 40-fold during development but were below detectable limits in KISS1-/- boars (age x genotype; P = 0.06). Androstenone and skatole in KISS1-/- boars (0.30 ± 1.24 µg/g and 12.6 ± 1.6 ng/g, respectively) at 190 d of age was less (P < 0.0001) than in KISS1+/+ and KISS1+/- boars (androstenone, 4.33 ± 1.16 µg/g; skatole, 69.2 ± 1.2 ng/g), which did not differ from one another. Thus, a single functional allele of KISS1 is sufficient to confer normal secretion of reproductive hormones, testicular growth, and skatole in boars. Moreover, knocking out the KISS1 gene will prevent boar taint, but might slightly reduce growth in later stages of development.