Exposure of dairy cows to high environmental temperatures and their lactation status impairs establishment of the ovarian reserve in their offspring

Abstract

The objectives of this study were to establish if exposure of pregnant dairy cows to high environmental temperatures and humidity during the first trimester of pregnancy impairs the establishment of the ovarian reserve (total number of healthy follicles and oocytes in ovaries) and fertility in their offspring. Serum anti-Müllerian hormone (AMH) concentrations and number of follicles ≥3 mm (antral follicle count; AFC) were assessed on a random day of the estrous cycle in 310 sixteen-month-old dairy heifers. Based on season of their conception and early fetal life, heifers were separated into 2 groups: summer (mean monthly temperature-humidity index = 69.33 ± 2.6) and winter (temperature-humidity index = 54.91 ± 1.08). The AMH and AFC were lower in summer (419.27 ± 22.81 pg/mL and 9.32 ± 0.42 follicles, respectively) compared with winter heifers (634.91 ± 47.60 pg/mL and 11.84 ± 0.46 follicles, respectively) and were not influenced by farm and age at sampling. Heifers born to dams that were not being milked during gestation had lower AMH and AFC compared with offspring of cows on their first lactation, whereas no difference was detected between offspring of cows on their first and subsequent lactations. Summer and winter heifers had similar age at first service and at first calving, and similar number of services per conception. Regardless of season in early fetal life, heifers were classified into 3 groups based on AMH and AFC (low = 20%, intermediate = 60%, high = 20%). Heifers with the lowest AMH were older at first service compared with herd mates with intermediate AMH, but age at first calving and number of services per conception were similar among AMH categories. No difference was detected in any of the fertility measures among AFC categories. Heifers born to mothers exposed to high environmental temperatures in early gestation had smaller ovarian reserves compared with herd mates conceived in winter, but no association between season of early fetal life and fertility at first conception was established. Season of conception and maternal lactation status affect the size of the ovarian reserve, but not fertility, at first conception in the progeny.

Developmental Programming of Fertility in Cattle—Is It a Cause for Concern?

“…In terms of daughter fertility, a THI ≥ 50 during this period was associated with longer intervals from calving to first insemination and the non-return-rate at 56 days after service decreased with increasing THI, confirming that heat stress can have an effect across generations. The effect of climate during the first trimester of pregnancy on ovarian reserves at 16 months of age was investigated by Succu et al [ 173 ] by comparing heifer offspring conceived during the summer (THI of 69) or winter (THI of 55). Both the AMH concentration and antral follicle count were lower in summer born compared with winter born heifers but this did not alter their subsequent fertility at first conception.…”

The ovarian follicle of ruminants: the path from conceptus to adult

“…Among the current gaps in our knowledge are the effects of maternal disease status and heat stress, both of which warrant more attention given the effects of global climate change on disease vectors and thermoregulation. Recently, it has been shown that dairy heifers conceived in the summer, with their mothers having been exposed to a high temperature-humidity index, had lower antral follicle counts and AMH concentrations than those conceived in the winter (Succu et al 2020), although there appeared to be no association between season and conception or fertility at first conception.…”

Association between maternal growth in the pre‐conception and early gestational period of nulliparous dairy heifers with anti‐Müllerian hormone in their female offspring

“…It has also been shown that dairy cows with chronically high somatic cell count may produce daughters with smaller ovarian reserves and suboptimal fertility as adults (Ireland et al, 2011). Maternal heat stress during the first trimester was shown to reduce AFC and AMH, but it did not affect subsequent first conception fertility measures (Succu et al, 2020).…”

“…AMH has been shown to be positively associated with antral follicle count (AFC) and ovarian reserve due to its origin in the granulosa cells (Alward et al., 2021; Ireland et al., 2011; Jimenez‐Krassel et al., 2015; Mossa et al., 2017; Succu et al., 2020) and is highly repeatable within animals, during and between oestrous cycles (Alward & Bohlen, 2020; Ireland et al., 2011; Jimenez‐Krassel et al., 2015; Karl et al., 2022; Mossa et al., 2017; Ramesha et al., 2022; Ribeiro et al., 2014; Souza et al., 2015; Umer et al., 2019). However, there is considerable variation between individual animals (Alward et al., 2021; Gobikrushanth et al., 2018; Ireland et al., 2011; Ramesha et al., 2022; Rico et al., 2012).…”