Markers of conceptus development reveal reduced developmental competence in pregnancies derived from lower SCR bulls

Differences in fertility among bulls are well documented in the field, yet the understanding of the male contributions to in vivo embryonic development and pregnancy outcomes remains ill-defined. This study aimed to evaluate the effect of sire fertility, based on sire conception rate (SCR), on the timing of pregnancy loss and markers of conceptus developmental capacity in vivo. Angus cows were artificially inseminated with semen from Holstein sires classified as HighSCR (n = 55) or LowSCR (n = 104). Day 0 (d0) was defined as the day of AI. Cervical cells were collected on d3, 14, 16, 18, and 20 to assess ISG15 mRNA abundance, and blood was collected on d3 and daily from d14 to d31 to determine progesterone and pregnancy-associated glycoproteins (PAG). Pregnancy outcomes were defined using ISG15 (d14), PAG (d23), and ultrasonography (d31). Pregnancy per AI was greater for HighSCR than LowSCR on d14 (96.4% vs 85.6%; P = 0.05), d23 (81.8% vs 61.5%; P = 0.01), and d31 (69.1% vs 50.0%; P = 0.02). Embryos derived from LowSCR had reduced developmental competence as evidenced by lower ISG15 abundance compared to HighSCR (42.3 ± 4.4 vs 61.6 ± 7.9; P = 0.04) and three-fold greater pregnancy loss particularly when trophoblast differentiation and attachment occurred on ≥d21. Additionally, pregnancy loss prior to d24 was most often (95%) associated with embryonic failure and luteal regression whereas pregnancy loss after d23 most often associated with conceptus failure without luteal regression (85%).