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We hypothesized the manner that heifers achieve puberty may indicate their future reproductive longevity. Heifers with discontinued or delayed cyclicity during puberty attainment may have irregular reproductive cycles, anovulation, and infertility in their first breeding season contributing to a shorter reproductive lifespan. Therefore, plasma progesterone (P4) was measured from weaning to breeding on 611 heifers born 2012–2017 and four pubertal classifications were identified: 1) Early; P4 ≥ 1 ng/ml < March 12 with continued cyclicity, 2) Typical; P4 ≥ 1 ng/ml ≥ March 12 with continued cyclicity, 3) Start-Stop; P4 ≥ 1 ng/ml but discontinued cyclicity, and 4) Non-Cycling; no P4 ≥ 1 ng/ml. Historical herd records indicated that 25% of heifers achieved puberty prior to March 12th in the 10 years prior to the study. Start-Stop and Non-Cycling yearling heifers were lighter indicating reduced growth and reproductive maturity traits compared to Early/Typical heifers. In addition, Non-Cycling/Start-Stop heifers were less responsive to prostaglandin F2 alpha (PGF2α) to initiate estrous behavior and ovulation to be artificially inseminated. Non-Cycling heifers had fewer reproductive tract score-5 and reduced numbers of calves born in the first 21-days-of-calving during their first breeding season. Within the Start-Stop classification, 50% of heifers reinitiated cyclicity with growth traits and reproductive parameters that were similar to heifers in the Early/Typical classification while those that remained non-cyclic were more similar to heifers in the Non-Cycling group. Thus, heifers with discontinued cyclicity or no cyclicity during puberty attainment had delayed reproductive maturity resulting in subfertility and potentially a shorter reproductive lifespan.

The UNL physiology herd has a population of cows that secrete excess androstenedione (A4) in follicular fluid. These High A4 cows are less fertile, have irregular cycles, are often anovulatory, and have similar characteristics to women with Polycystic Ovary Syndrome (PCOS). Ovarian cortex cultures of High A4 cows secrete more A4 than controls. High A4 cows reached puberty 45 d earlier than control cows. Thus, we hypothesized that heifers reaching puberty earlier were predisposed to become High A4 cows. To test this hypothesis, we collected blood plasma from weaning to breeding (2012–2017) in 611 heifers. A custom SAS program was developed using progesterone >1ng/ml to identify four distinct puberty groups: 1) Early Puberty- 317.0 ± 3.6 days of age (doa) with continued cyclicity (n = 143); 2) Typical Puberty- 378.4 ± 2.1 doa with continued cyclicity (n = 279); 3) Start-Stop Puberty- 265.3 ± 4.1 doa with discontinued cyclicity (n = 91); and 4) Non-Cycling- no P4≥1ng/ml (n = 98). The pattern of Sex Hormone Binding Globulin (SHBG) was increased prior to puberty in Early and Typical and reduced in Start-Stop and Non-Cycling heifers. Early heifers (4.9) had greater prebreeding reproductive tract scores, followed by Typical (4.7), Start-Stop (4.5), and Non-Cycling (4.0) heifers. At breeding, all heifers that showed estrus in response to PGF2a were artificially inseminated. Typical (78.9%), Early (79.5%) and Start-Stop heifers (50.3%) had a greater response compared to Non-Cycling heifers (12.6%). All heifers were exposed to bulls, and overall pregnancy rate was not different. However, a greater percentage of Typical (57.9%), Early (51.0%), and Start-Stop (45.2%) heifers calved in the first 21 d of the calving season compared to Non-Cycling (20.9%). Start-Stop (3.0ng/ml) and Non-Cycling (4.2ng/ml) heifers had increased A4 in ovarian cortex culture media compared to Typical (0.062ng/ml) or Early (0.091ng/ml) puberty heifers. Greater A4 produced by ovarian cortex of Start-Stop and Non-Cycling heifers, irregular cycles and reduced calves in the first 21 d indicates these females may be predisposed to becoming High A4 cows with decreased fertility.

Follicular progression during peripuberty is affected by diet. Vascular endothelial growth factor A (VEGFA) induces follicle progression in many species; however, there are limited studies to determine if diet may alter the effects of angiogenic VEGFA165-stimulated follicle progression or antiangiogenic VEGFA165b follicle arrest. We hypothesized that diet affects the magnitude of angiogenic and antiangiogenic VEGFA isoform actions on follicular development through diverse signal transduction pathways. To test this hypothesis, beef heifers in our first trial received Stair-Step (restricted and refeeding) or control diets from 8 to 13 months of age. Ovaries were collected to determine follicle stages, measure vascular gene expression and conduct ovarian cortical cultures. Ovarian cortical cultures were treated with phosphate-buffered saline (control), 50 ng/ml VEGFA165, VEGFA165b, or VEGFA165 + VEGFA165b. The Stair-Step heifers had more primordial follicles (P < 0.0001), greater messenger RNA abundance of vascular markers VE-cadherin (P < 0.0001) and NRP-1 (P < 0.0051) than controls at 13 months of age prior to culture. After culture, VEGFA isoforms had similar effects, independent of diet, where VEGFA165 stimulated and VEGFA165b inhibited VEGFA165-stimulated follicle progression from early primary to antral follicle stages. In vitro cultures were treated with VEGFA isoforms and signal transduction array plates were evaluated. VEGFA165 stimulated expression of genes related to cell cycle, cell proliferation, and growth while VEGFA165b inhibited expression of those genes. Thus, VEGFA isoforms can act independently of diet to alter follicle progression or arrest. Furthermore, follicle progression can be stimulated by VEGFA165 and inhibited by VEGFA165b through diverse signal transduction pathways.

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