Impact of paternal high energy diets on semen quality and embryo development in cattle

Abstract

Highly anabolic diets and excessive body fat accumulation have been shown to negatively impact sperm biology in humans and murine biomedical models. Current research indicates that obesity is associated with decreased semen quality and represents a major contributor to male subfertility in humans. Male overnutrition is commonly observed in the beef cattle industry and the use of high energy diets during bull development has been shown to negatively impact semen quality. Most research efforts in bovine reproductive physiology have focused on understanding and optimizing female fertility. This emphasis is even more evident in research investigating the relationship between nutritional interventions and reproductive performance, which has limited the development of nutritional strategies that optimize fertility in bulls. Increasing our understanding of the genetic and environmental factors that influence bull fertility will contribute to future increases in cattle reproductive and productive efficiency. Moreover, exploring the impact of overnutrition in bulls may offer valuable insight and help address diet-induced male subfertility in humans. Herein, we summarize the currently available literature evaluating the impact of highly anabolic diets on male fertility, with an emphasis in the bovine species. Literature summarized in the present review evaluates the impact of overnutrition on sperm biology, early embryonic development, and explores its potential to impact postnatal performance of the offspring.

Figure 1

Bulls were fed their respective diet for 168 days at which time scrotal circumference (A), sperm motility (B) or secondary sperm defects (C) were evaluated. Control: moderate-gain diet. HG, high-gain diet. SC, Scrotal circumference. a, b superscript differ: P < 0.05 for all panels. Adapted from Coulter et al.(1997).

Figure 2

Relationship between subcutaneous backfat thickness and sperm morphology in growing beef bulls that were exposed to the same diet. Bulls were retrospectively ranked based on subcutaneous backfat thickness as top, medium or bottom 10 or 20% of the population for subcutaneous backfat thickness. a, b superscript differ: P ≤ 0.05 for all panels. BSE, breeding soundness examination. Bulls were considered to have failed the BSE when morphologically normal cells were <70% according to the Society of Theriogenology. Adapted from Smith et al. (2024).

Figure 3

Fresh and frozen-thawed semen from bulls fed either a maintenance (ADG = 0.02 kg/day) or a high-gain diet (ADG = 1.97 kg/day) were analyzed using flow cytometry for acrosomal integrity (A), early necrosis (B) and viability (C). Different superscripts indicate statistical differences (P ≤ 0.05) and symbols indicate a tendency (P < 0.10; Seekford et al. 2023).

Figure 4

Oocytes were fertilized using semen from bulls fed either a maintenance (ADG = 0.02 kg/day) or a high-gain diet (ADG = 1.97 kg/day). Zygote cleavage was assessed at day 3 postfertilization (A). The percentage of oocytes (B) and cleaved oocytes (C) that formed blastocysts were analyzed 7.5 days after fertilization (Seekford et al. 2023).

Figure 5

(A) Plasma concentrations of PAGs in cows that had a viable pregnancy on day 30 of gestation, but experienced pregnancy loss by day 100 of gestation. (B) Plasma PAG on day 30 of gestation in cows that maintained pregnancy and were sired by bulls that induce high (HPL) or low rates of pregnancy loss (LPL). (C) Plasma PAGs from cows receiving parthenogenome (PA; no male pronuclei) or control embryos (treatment × time; P ≤ 0.05). a,b superscript differ (P ≤ 0.05). Adapted from Franco et al. (2018) and Singleton et al. (2023).

Figure 6

Summary of potential consequences of paternal overnutrition to gamete quality, embryo development and paternal programming of the offspring. Bolded items represent the consequences of sire overnutrition that have been reported in the bovine, whereas non-bolded items represent consequences reported in other species. ROS, reactive oxygen species. Figure was generated using BioRender.