J. Dairy Sci.

103:1685–1700
https://doi.org/10.3168/jds.2019-17374
© 2020, The Authors. Published by FASS Inc. and Elsevier Inc. on behalf of the American Dairy Science Association®.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Reproductive efficiency and survival of Holstein-Friesian

cows of divergent Economic Breeding Index, evaluated
under seasonal calving pasture-based management
M. O’Sullivan,1,2 S. T. Butler,1 K. M. Pierce,2 M. A. Crowe,3 K. O’Sullivan,4 R. Fitzgerald,1
and F. Buckley1,2*
1
Animal and Grassland Research and Innovation Centre, Teagasc Moorepark, Fermoy, Co. Cork, P61 C997, Ireland
2
School of Agriculture and Food Science, University College Dublin, Belfield, Dublin, D04 N2E5, Ireland
3
School of Veterinary Medicine, University College Dublin, Belfield, Dublin, D04 N2E5, Ireland
4
School of Mathematical Sciences, University College Cork, Cork, T12 XF62, Ireland

ABSTRACT than NA by the beginning of the fifth lactation. The

results highlight the success of the Economic Breeding
The objective of the current study was to examine Index to deliver reproductive performance and longev-
phenotypic fertility performance and survival, and to ity consistent with industry targets across a range of
gain insight into underlying factors that may contribute seasonal pasture-based FT. The results also clearly
to greater fertility performance in 2 divergent genetic demonstrate the potential of appropriate genetic selec-
groups (GG) of Holstein-Friesian, selected using the tion to reverse negative fertility trends incurred during
Irish Economic Breeding Index (EBI). The GG were previous decades of selection for milk production alone.
evaluated across 3 spring calving pasture-based feeding Key words: dairy cow, Economic Breeding Index,
treatments (FT) over 4 yr. The 2 divergent GG were Holstein-Friesian, reproductive efficiency
(1) high EBI; representative of the top 5% nationally
(elite), and (2) EBI representative of the national aver-
INTRODUCTION
age (NA). In each year, 90 elite and 45 NA cows were
randomly allocated to 1 of 3 FT: control, lower grass The efficiency of seasonal calving pasture-based milk
allowance, and high concentrate. No interaction be- production systems is dependent on achieving synchro-
tween GG and FT was observed for any of the measures ny between feed demand and pasture growth (Shalloo
of fertility investigated. The elite cows achieved sig- et al., 2007). Maintaining compact calving is a major
nificantly greater pregnancy rate to first service (+14.9 challenge within pasture-based dairying (Macmillan,
percentage points), and significantly greater pregnancy 2012), requiring consistent achievement of excellent
rates after 21, 42, and 84 d of breeding (+17.3, +15.2, levels of reproductive performance (O’Farrell, 1994;
and +9.6 percentage points, respectively) compared McDougall, 2006). Failure to maintain compact calving
with NA. The number of services per cow was fewer results in financial losses due to reduced pasture utili-
for elite (1.57) compared with NA (1.80). The interval zation, increased costs associated with higher replace-
from mating start date to pregnancy was significantly ment rate (Shalloo et al., 2014), and milk production
shorter for elite cows compared with NA. The elite cows losses associated with immature herd parity structure
maintained greater mean body condition score than NA (Pritchard et al., 2013).
throughout the study (2.91 vs. 2.72), and had greater Declining fertility performance, identified through
body condition score at calving, artificial insemination, controlled research (Snijders et al., 2001; Kennedy et
and drying off compared with NA. The elite cows had al., 2002) and research conducted at the commercial
greater mean circulating concentrations of insulin-like farm level in Ireland (Evans et al., 2006), prompted the
growth factor-1 compared with NA. No significant ef- development and implementation of a national breeding
fect was observed of GG on commencement of luteal objective, the Economic Breeding Index (EBI). The
activity, or progesterone profile variables. Greater sur- EBI incorporates selection for fertility and production,
vival to the start of fifth lactation was observed for elite simultaneously reflecting the demands of seasonal calv-
cows. The elite cows were 43% less likely to be culled ing systems (Veerkamp et al., 2002). Seasonal calving
pasture-based systems are relatively unique and ac-
count for a small proportion of global milk production
Received July 31, 2019.
Accepted October 13, 2019. (~10%; Steinfeld and Mäki-Hokkonen, 1995), and thus,
*Corresponding author: Frank.Buckley@​teagasc​.ie the majority of dairy cattle worldwide have not been
1685
 O’Sullivan et al.: REPRODUCTIVE EFFICIENCY AND SURVIVAL OF COWS 1686

selected under grazing conditions. Although fertility tion Herd were described in detail by O’Sullivan et al.
has recently gained greater emphasis in the selection in- (2019b). Briefly, the 2 GG compared were high EBI,
dices in most countries (Miglior et al., 2005, 2017), the within the top 5 percentile of cows nationally, ranked
emphasis on fertility and survival varies widely (Miglior on EBI (elite), and cows representative of the national
et al., 2012; Cole and VanRaden, 2018) and there is no average genetic merit (NA). The mean EBI and EBI
consensus in trait definition or methodology for evalu- sub-index values for milk, fertility, calving, beef, main-
ation (Miglior et al., 2017). Hence, although worldwide tenance, health, and PTA for calving interval and sur-
genetic trends suggest a reversal in the rate of genetic vival, for the elite and NA cows, excluding the influence
deterioration of fertility traits, improvement in the of both own and progeny performance, are summarized
phenotypic fertility performance trend is not evident in Table 1 (ICBF, 2018). Each year, 90 elite and 45 NA
in all countries (Pryce et al., 2014). Strong emphasis is cows were randomly assigned in mid-March and mid-
placed on fertility and survival (35%) within the Irish April, for the early and late calving cows, respectively,
EBI. Genotypic and phenotypic fertility trends in Irish to 1 of 3 experimental feeding treatments (FT). Both
herds during the past decade indicate improvement GG were balanced for parity and calving date each
(ICBF, 2018), but mean performance at farm level is year. The 3 experimental FT were control (CTL), high
still behind industry targets (O’Farrell, 1994; McDou- concentrate (HC), and lower grass allowance (LGA),
gall, 2006). characterized by target postgrazing compressed sward
The Next Generation Herd was established at Tea- heights of 4.5 to 5 cm, 4.5 to 5 cm, and 3.5 to 4 cm,
gasc, Moorepark, as a sentinel research herd to investi- and planned concentrate allowances of 300, 1,100, and
gate the anticipated phenotypic performance of futur- 300 kg per cow per year, respectively. The 3 FT were
istic animals selected using EBI. Previous results from designed to represent management scenarios reflective
the Next Generation Herd study indicate favorable ge- of the upper and lower limits of recommended best
netic gain for milk solids yield, BCS, and the utilization practice to maximize productivity in Irish milk produc-
of ingested energy in cows with high EBI compared tion systems (O’Donovan et al., 2011). Details of the
with cows with low EBI (O’Sullivan et al., 2019a). The pasture management and grass quality were reported
objective of the present study was to examine pheno- by O’Sullivan et al. (2019a,b).
typic fertility performance and survival, and to gain
insight into underlying factors that may contribute to Reproductive Management
greater fertility performance in cows selected for high
EBI. We tested the hypothesis that genetic selection Before the mating start date (MSD) each year, all
for high EBI results in greater reproductive efficiency cows greater than 30 DIM were examined using tran-
and longevity. srectal ultrasonography (Ibex Pro scanner with an 8.5
MHz transducer, E.I. Medical Imaging, Loveland, CO)
MATERIALS AND METHODS to assess uterine and ovarian status. The incidence of
reproductive disorders (endometritis, pyometra, ovarian
This study was carried out at the Dairygold Research cysts, anovulatory anestrus) was recorded. Intervention
Farm (Teagasc, Animal and Grassland Research and to treat anovulatory anestrous cows was not under-
Innovation Centre, Moorepark, Fermoy, Co. Cork, Ire-
land; 52°09′N; 8°16′W) over a 4-yr period (2013–2016).
Experimental procedures involving animals in the pres- Table 1. The mean and SD of Economic Breeding Index (EBI), EBI
ent study were licensed by the Health Products and sub-indexes, and PTA for fertility traits of the 2 genetic groups of
Regulatory Authority as per the project authorization Holstein-Friesian studied1
AE19132/P023, in accordance with the Cruelty to Item Elite (SD) NA (SD)
Animals Act (Ireland 1876, as amended by European
EBI 154 ± 34.2 47 ± 30.9
Communities regulations 2002 and 2005; Department Sub-index    
of Health and Children, Ireland, 2005) and the Eu-   Milk (€) 28 ± 20.0 7± 17.5
ropean Community Directive 86/609/EC (Council of   Fertility (€) 103 ± 28.9 28 ± 22.7
  Calving (€) 31 ± 8.0 24 ± 8.6
the European Union, 1986), and were approved by the   Beef (€) −21 ± 7.6 −13 ± 8.0
Teagasc Animal Ethics Committee.   Maintenance (€) 12 ± 8.5 2± 8.9
  Health (€) 0± 4.6 −1 ± 4.6
PTA    
Animals and Feeding Treatments   Calving interval (d) −5.2 ± 1.74 −1.21 ± 4.6
  Survival (%) 3.13 ± 1.01 1.14 ± 0.91
Two genetic groups (GG) of Holstein-Friesian (HF) 1
Genetic group of Holstein-Friesian: Elite = high EBI; NA = national
cows were compared. The GG within the Next Genera- average EBI.

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taken before wk 7 of the breeding season to allow cows (Preg42; proportion of cows that became pregnant
express their inherent reproductive potential. A total of during the first 42 d of the breeding season confirmed
9 anovulatory anestrous cows received a progesterone- by ultrasound scans during and after the end of the
ovsynch protocol, previously described by (Cummins et breeding season); 84-d pregnancy rate (Preg84; pro-
al., 2012a), after wk 7 of the breeding season over the portion of cows pregnant by d 84 of the breeding season,
4 yr (6 elite, 3 NA; 0.03 of each GG). All experimental confirmed by ultrasound scan 80 d after the end of the
animals were tail-painted twice weekly as part of the breeding season); MSD to first-service interval; MSD
normal management practice to aid identification of to pregnancy interval; services per cow (number of
estrous events, commencing 3 wk before MSD. During times each cow was served during the breeding season);
the breeding season, heat detection was carried out a embryonic loss (proportion of cows that did conceive
minimum of 3 times daily with the aid of tail paint, (pregnant at 30 to 36 d postservice) but did not remain
and activity monitoring collars (MooMonitor, Dairy- pregnant (nonpregnant at 60 to 66 d postservice, or
master, Causeway, Co. Kerry, Ireland) were fitted to after the end of the breeding season).
each animal before parturition. The breeding season
commenced on April 25 of each year, and lasted for 12 BW and BCS
wk. Cows that were observed standing to be mounted,
or that had tail paint removed and showed physical Body weight was recorded weekly using calibrated
signs of estrus, were drafted for AI. During wk 1 to electronic scales (Dairymaster, Causeway, Co. Kerry,
6 of the breeding season, cows detected in heat were Ireland). Body condition score was recorded every 2
inseminated with frozen-thawed semen from a bull, wk in early lactation (up to wk 10 of lactation), and
chosen from a team of genomically selected young sires approximately every 3 to 4 wk thereafter by a single
of the highest EBI. The same team of bulls was used evaluator. The scale used was 1 to 5 (with 1 being
across both GG. Cows displaying estrus during the extremely thin and 5 being extremely fat), with incre-
breeding season were inseminated regardless of calving ments of 0.25 (Edmonson et al., 1989). Variables calcu-
date and the same inseminator performed all AI events lated included BW and BCS at calving (measured on
for each year of the study. Cows detected in estrus the week of calving or less than 2 wk before calving),
were inseminated once daily, after morning milking. BW and BCS nearest AI, and BW and BCS at the end
For each sire used, semen was from a single ejaculate, of lactation. The week of BCS nadir was determined by
and sperm viability and quality were verified before use identifying the earliest postpartum occurrence of the
in the experiment. During wk 7 to 12 of the breeding lowest BCS value recorded during the first 15 wk of
season, natural service was carried out by easy-calving lactation. Changes in BCS from calving to BCS nearest
Aberdeen Angus bulls. Bulls underwent a breeding AI, and from the BCS nearest AI to end of lactation,
soundness evaluation before joining the experimental were calculated.
herds. Pregnancy diagnosis was carried out by tran-
srectal ultrasound at 30 to 36 d and again at 60 to 66 Blood Metabolite and Hormone Analysis
d postinsemination to determine pregnancy status and
embryo loss. Final pregnancy status was determined by Blood samples were collected via coccygeal veni-
transrectal ultrasound 80 d after the completion of the puncture using 21-gauge vacutainer needles into 10-mL
breeding season. These ultrasound examination records lithium heparin vacutainer tubes (Becton Dickinson,
were used to assign a pregnancy date for every cow. Plymouth, UK). All blood samples were centrifuged at
1,500 × g for 15 min at 4°C; the plasma was harvested
Reproductive Measurements and aliquoted into two 3.5-mL plasma tubes (Sarstedt,
Nümbrecht, Germany) and stored at −20°C until later
The reproductive measurements that were calculated analysis. Plasma samples collected at wk −2, 1, 2, 3 4,
were as follows: 21-d submission rate; proportion of all 6, 8, and 10 relative to parturition were analyzed for
cows inseminated within the first 21 d of the breeding concentrations of plasma fatty acids, BHB, and glucose
season; pregnancy rate to first service (proportion of by enzymatic colorimetry using an ABX Pentra 400
cows pregnant to first service confirmed by ultrasound autoanalyzer (ABX Mira, Montpellier, France; fatty
scan during and after the end of the breeding season); acids kit supplied by Wako Chemicals GmBH, Neuss,
21-d pregnancy rate (Preg21; proportion of cows that Germany; BHB kit supplied by Randox Laboratories
became pregnant during the first 21 d of the breeding Limited, Crumlin, Co. Antrim, United Kingdom; Glu-
season confirmed by ultrasound scans during and after cose kit supplied by Horiba ABX, Montpellier, France).
the end of the breeding season); 42-d pregnancy rate Plasma samples collected at wk −2, 1, 2, 4, 6, 8, and 10

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 O’Sullivan et al.: REPRODUCTIVE EFFICIENCY AND SURVIVAL OF COWS 1688

relative to parturition were analyzed for concentrations Statistical Analysis

of insulin and IGF-1. Concentrations of insulin were
determined using an immunoradiometric assay (DIA- All statistical analyses were carried out using SAS
source ImmunoAssays, Louvain-la-Neuve, Belgium). (version 9.4, SAS Institute Inc., Cary, NC). The effect
Concentrations of IGF-1 were determined using a vali- of GG was of primary interest in the current study.
dated double antibody RIA following ethanol: acetone: The timing of FT implementation meant the effect of
acetic acid extraction (Beltman et al., 2010). Inter- and FT on blood metabolites and hormonal status, particu-
intraassay coefficients of variation were 3.6 and 7.5% larly in the early lactation period, was not captured.
for insulin and 4.4 and 10.8% for IGF-1, respectively. However, the effect of FT was included in all statistical
models for completeness and its interaction with GG
Milk Progesterone was considered. The effect of GG on variables with
repeated measures, such as BCS, BW, and blood me-
Milk samples were collected using electronic milk tabolite and hormone concentrations, was determined
meters (Dairymaster, Causeway, Co. Kerry, Ireland), using mixed models. The effects of GG, FT, parity,
during the p.m. milking 3 times/wk (Monday, Wednes- calving date, year, lactation, week, and their interac-
day, Friday) from parturition until wk 5 after MSD tions were included in the final model where significant
for progesterone (P4) analysis to determine interval (P < 0.05), with cow nested within GG included as
from calving to resumption of cyclicity and estrous a random effect. Each model was tested using 4 dif-
cycle characteristics. After milking, samples were ali- ferent covariance structures (autoregressive order one,
quoted into 96-well MegaBlocks (Sarstedt, Nümbrecht, autoregressive order one with heterogeneous variance,
Germany) and stored at −20°C until P4 analysis. Milk compound symmetry, and unstructured). The model
P4 concentrations were measured using an ELISA and covariance structure with the lowest Akaike’s
(Ridgeway Science, Gloucestershire, UK). Cows were information criterion was used to identify the most
considered to have an active corpus luteum when milk appropriate residual covariance structure for repeated
P4 concentrations exceeded 3 ng/mL. Using the milk measures. A compound symmetry error structure was
P4 profile, estrous cycle characteristics including the determined as the most appropriate residual covariance
commencement of luteal activity (C-LA), luteal phase structure for repeated measures. Plasma IGF-1, fatty
(LP) duration, inter-ovulatory interval (IOI), inter- acids, and BHB concentrations were transformed to
luteal interval (ILI), delayed ovulation type I (DOVI), generate a normal distribution and the estimated group
delayed ovulation type II (DOVII), persistent corpus means and 95% confidence intervals were derived from
luteum type I (PCLI), and persistent corpus luteum back-transformed values. The final model used was
type II (PCLII) were calculated for each individual
cow as previously described (Horan et al., 2005). Rijklm = μ + Yi + Gj + Fk + Ll + Wm
+ Gj × Wm + eijklm,
Survival Analysis

Data from cows that participated in the study be- where Rijklm = the observation for the dependent vari-
tween 2013 and 2016 were included in the survival able (BW, BCS, insulin, IGF-1, glucose, fatty acids,
analysis, including cows that had left the experimental and BHB concentrations); Yi = the effect of ith year (i
herd (i.e., surplus cows and those sold to commercial = 1, 2, 3, 4); Gj = the effect of the jth genetic group (j
herd-owners). Date and reason for culling were re- = elite, NA); Fk = the effect of the kth feeding treat-
corded for all animals. Re-calving and survival data for ment (k = CTL, HC, LGA); Ll = the effect of the lth
all cows that participated in the study between 2013 parity, Wm = the effect of the mth week of lactation; Gj
and 2016 were extracted from the Computerised Cattle × Wm = the interaction between genetic group j and
Movement Monitoring System database operated by lactation week m, and eijklm = the residual error term.
the Department of Agriculture, Food and the Marine. The effect of GG on continuous variables without
A total of 122 elite and 55 NA animals were pregnant repeated measures such as MSD to first-service inter-
at the end of the study; these animals were assumed val, MSD to pregnancy interval, number of services per
censored on the last day of 2016, as their ultimate cow, and selected BW and BCS variables (i.e., BW and
survival time was unknown. All animals culled due BCS at calving, postpartum BW and BCS nadir, week
to infertility were assigned the status of culled on the of BCS nadir, BW and BCS nearest AI, BW and BCS
date of drying off at the end of lactation. Survival was at the end of lactation, and changes in BW and BCS
defined as the numbers of days from first calving to the from calving to AI, calving to nadir, and from nadir
date of culling. to end of lactation) were determined using a mixed
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 O’Sullivan et al.: REPRODUCTIVE EFFICIENCY AND SURVIVAL OF COWS 1689

model (PROC MIXED; SAS Institute Inc.) with cow the effect of the kth feeding treatment (k = CTL, HC,
nested within GG as a random effect. The effect of GG, LGA); Ll = the effect of the lth parity, and eijkl = the
FT, parity, and their interactions were tested, calving residual error term.
date and year were included as adjustment variables. Data from 272 cows (177 elite, 95 NA) that entered
Interactions that were nonsignificant (P > 0.05) were the study were included in the survival analysis. Kaplan-
eliminated from the final model: Meier survival probabilities were derived by defining
GG as strata in PROC LIFETEST. Differences in the
Rijkl = μ + Yi + Gj + Fk + Ll + eijkl, survival experience of both GG were estimated using
the log-rank test. The effect of GG on cow survival
where Rijkl = the observation on the animal for the de- was analyzed by the Cox proportional hazards model
pendent variable (BW and BCS at calving, postpartum using PROC PHREG of SAS. Effects were expressed
BW and BCS nadir, week of BCS nadir, BW and BCS as relative hazard ratios. The elite were the reference
nearest AI, BW and BCS at the end of lactation, and class (i.e., their hazard ratio was set to 1). Therefore, a
changes in BW and BCS from calving to AI, calving to relative hazard ratio greater than 1 indicates a higher
nadir, and from nadir to the end of lactation) in year i, risk of culling (i.e., lower survivability).
of parity j, and genetic group k, on feeding treatment
l; Yi = the effect of ith year (i = 1, 2, 3, 4); Gj = the RESULTS
effect of the jth genetic group (j = elite, NA); Fk =
the effect of the kth feeding treatment (k = CTL, HC, Reproduction and Fertility
LGA); Ll = the effect of the lth parity, and eijkl = the
residual error term. Mean calving date over the 4-yr study period was
Differences between GG for variables with a binomial February 15 (±16 d) and 18 (±18 d) for elite and NA
distribution (21-d submission rate, pregnancy rate to cows, respectively, and the calving period ranged from
first service, Preg21, Preg42, and Preg84) were tested January 6 to April 12. The interaction between GG
using generalized linear mixed models (PROC GLIM- and FT was not significant for any of the fertility vari-
MIX), with a binary distribution specified in the model ables investigated, and was therefore omitted from final
statement. The final model was statistical models. The effect of GG on reproductive
performance is summarized in Table 2. Pregnancy rate
Rijkl = μ + Yi + Gj + Fk + Ll + eijkl, to first service, Preg21, Preg42, and Preg84 was greater
(+14.9, +17.3, +15.2, and +9.6 percentage points, re-
where Rijkl = the observation on the animal for the spectively; P < 0.001) for elite compared with NA. The
dependent variable (21-d submission rate, pregnancy number of services per cow was fewer (P < 0.01) for
rate to first service, Preg21, Preg42, and Preg84) in elite compared with NA. While numerically lower for
year i, and genetic group j, on feeding treatment k, of elite, the proportion of embryo mortality did not differ
parity l; Yi = the effect of ith year (i = 1, 2, 3, 4); Gj = significantly between elite and NA. The interval from
the effect of the jth genetic group (j = elite, NA); Fk = MSD to first service tended to be shorter for elite cows

Table 2. The effect of genetic group (GG) of Holstein-Friesian dairy cow on reproductive performance during
a 12-wk breeding season1

GG

Item Elite NA SEM P-value

21-d submission rate (%) 93.2 88.1 — 0.07
Pregnancy rate to first service (%) 60.4 45.5 — 0.001
Preg21 (%) 53.1 35.7 — 0.001
Preg42 (%) 72.7 57.5 — 0.001
Preg84 (%) 92.7 83.1 0.02 0.01
MSD to first service interval (d) 13.8 16.0 0.85 0.07
MSD to pregnancy interval (d) 25.3 31.1 1.55 0.01
No. of services per cow 1.57 1.80 0.06 0.01
Embryo mortality (%) 3.8 6.4 — 0.27
1
Elite = high Economic Breeding Index; NA = national average Economic Breeding Index; Preg21 = 21-d
pregnancy rate; Preg42 = 42-d pregnancy rate; Preg84 = 84-d pregnancy rate; MSD = mating start date.

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(P = 0.07), and the interval from MSD to pregnancy Circulating Concentrations of Blood Metabolites
was significantly shorter (−5.8 d; P < 0.01) for elite and Metabolic Hormones
cows compared with NA.
The temporal profiles of circulating blood metabo-
lites and hormones during the prepartum and early lac-
BW and BCS
tation period (wk −2 to 10) are illustrated in Figures 3
The BW profile of both GG from wk −2 to 42 of and 4, respectively. Interactions between GG and week
lactation is illustrated in Figure 1. Mean BW (Table were not significant for glucose, BHB, or fatty acids. A
3) was greater for NA cows compared with elite (+12 tendency for greater plasma glucose concentrations was
kg, P < 0.01). A significant GG by week interaction for observed for elite animals compared with NA (70.3 ±
BW (P < 0.05) was observed. A tendency was observed 0.8 vs. 68.2 ± 1.01 mg/dL; P = 0.07). The elite cows
for greater BW at calving for NA cows compared with had lower circulating BHB concentrations compared
elite (P = 0.08). Body weight at AI (P < 0.05) and with NA (0.91 ± 0.004 vs. 0.93 ± 0.006 mmol/L; P
BW at drying off (P < 0.05) were greater for NA cows = 0.04). The NA cows had lower circulating fatty acid
compared with elite. Body weight changes from calving concentrations compared with elite (0.86 ± 0.003 vs.
to AI, calving to nadir, and nadir to drying off did not 0.87 ± 0.005 mmol/L; P = 0.04). The elite cows had
differ significantly between elite and NA. Elite cows greater mean circulating concentrations of IGF-1 com-
maintained greater mean BCS (+0.19 units, P < 0.001) pared with NA (109.87 ± 34.92 vs. 99.96 ± 38.07 ng/
throughout the study compared with NA (Table 3). No mL; P = 0.002). A tendency for higher mean circulating
interaction was observed between GG and FT detected concentrations of plasma insulin was observed for elite
for BCS (P = 0.33). The elite cows had greater BCS cows during the sampling period (P > 0.06). A GG
at calving, nearest AI, and drying off compared with by time interaction was observed for insulin. The elite
NA. The elite cows had greater BCS at nadir (P < cows had greater circulating concentrations of insulin
0.001). No significant differences were observed for the (P < 0.01) at 2 wk before parturition, but postpartum
week of lactation when nadir BCS occurred. Changes insulin concentrations did not differ.
in BCS from parturition to nadir, and from nadir to
drying off did not differ significantly between GG. The P4 Profiles
BCS profile of both GG from wk −2 to 42 of lacta-
tion is illustrated in Figure 2. No significant interaction No significant effect was observed of GG on C-LA,
between GG and week of lactation was observed (P = first and second LP length, first and second ILI, and
0.11). first and second IOI (Table 4). The number of luteal

Figure 1. The mean BW profile of high Economic Breeding Index (elite) and national average Economic Breeding Index (NA) cows during
the gestation-lactation cycle. Data are presented as LSM, and error bars represent the SEM. The NA cows maintained greater mean BW (P <
0.01; SEM = 3.70) than elite cows from prepartum to the end of the lactation.

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phases in the first 60 d postpartum did not differ sig- traits (Miglior et al., 2017; Cole and VanRaden, 2018).
nificantly between GG. Peak P4 concentration during Genomic selection has accelerated the rate of genetic
the first and second luteal phases did not differ signifi- progress in dairy cows (Bouquet and Juga, 2013), but
cantly between GG. The incidence of DOVI, DOVII, rapid progress can lead to unexpected outcomes (Lucy,
PCLI, and PCLII was 7.3, 1.6, 2.8, and 1.0% for elite 2019). Historical selection for high milk production has
cows and 7.8, 0.4, 3.1, and 1.5% for NA cows. Genetic been associated with deterioration in fertility (Pryce
group had no significant effect (P < 0.05) on any of the et al., 2004), and has been reported in several studies
ovarian disorders investigated. (Snijders et al., 2001; Washburn et al., 2002; Veerkamp
et al., 2003; Evans et al., 2006). Controlled experiments
Survival on animals divergent for the breeding goal can be effi-
ciently used to elucidate the expected responses to selec-
Age at first calving for the elite and NA was 667 d tion for difficult or expensive-to-measure traits (Berry,
(SD 35.3), and 651 d (SD 57.8), respectively. Figure 5 2015). For example, greater fertility performance has
illustrates the survival curves to the beginning of the been observed in strains of HF selected under grazing
5th lactation over the study period for each GG. A total conditions compared with strains sourced from largely
of 59.3% of the elite, and 38.7% of the NA were treated confinement systems (Horan et al., 2004; McCarthy et
as right censored in the data set due to unknown final al., 2007a). Furthermore, Cummins et al. (2012a,b) and
survival time after completion of the current study. The Moore et al. (2014) validated a novel lactating Hol-
elite were 43% less likely to be culled than NA (P < stein-Friesian cow model of fertility, identifying a range
0.01) by the beginning of the fifth lactation. of physiological factors that differ between cows with
good or poor genetic merit for fertility traits. These
DISCUSSION included BCS, hormones and energy metabolites, and
ovarian function.
Dairy cow selection indices have changed markedly
during the last 25 yr (Lucy, 2019). Selection objec- Reproductive Efficiency
tives have evolved from single trait selection for milk
production to multi-trait selection incorporating many The superior reproductive performance observed in
nonyield traits such as fertility, health, and fitness elite cows in the present study is consistent with greater

Table 3. The effect of genetic group (GG) of Holstein-Friesian on mean BW and BCS variables1

GG P-value

Variable Elite NA SEM GG GG × week

BW          
  Mean BW (kg) 534.6 546.6 3.70 <0.01 <0.05
  BW at calving2 (kg) 595.1 607.3 5.13 0.08 —
  BW nearest AI (kg) 514.3 524.5 3.86 <0.05 —
  BW at the end of lactation (kg) 575.4 589.5 4.37 <0.05 —
BW change         —
  Calving to AI (kg) 81.4 84.2 4.23 0.63 —
  Calving to nadir (kg) 43.1 38.2 2.18 0.10 —
  Nadir to end of lactation (kg) 106.0 110.8 2.93 0.19 —
BCS          
  Mean BCS 2.91 2.72 0.16 <0.001 0.11
  BCS at calving3 3.25 3.03 0.03 <0.001 —
  BCS nearest AI 2.92 2.75 0.02 <0.001 —
  BCS at the end of lactation 2.96 2.70 0.02 <0.001 —
  BCS at nadir 2.85 2.63 0.03 <0.001 —
  Week of nadir (wk) 9.8 10.2 1.35 0.77 —
BCS change         —
  Calving to AI 0.33 0.28 0.03 0.52 —
  Calving to nadir 0.40 0.41 0.03 0.97 —
  Nadir to end of lactation 0.11 0.7 0.03 0.26 —
1
Elite = high Economic Breeding Index; NA = national average Economic Breeding Index.
2
BW at calving was the BW measured less than 2 wk before calving.
3
BCS at calving was the BCS measured on the week of calving or less than 2 wk before calving.

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genetic merit for fertility traits in the elite GG. The fertility traits within selection objectives is required if
reproductive performance achieved by the elite cows improvements in phenotypic fertility performance are
in the present study was consistent with recommended required in the short to medium term.
industry targets (O’Farrell, 1994; McDougall, 2006),
whereas the NA cows did not achieve the industry BW and BCS
targets. The reproductive performance achieved by
the elite cows indicates substantial genetic progress The lower mean BW of elite cows compared with
in genetic and phenotypic fertility has been achieved, NA cows in the present study is consistent with their
reversing the trends previously reported at the same greater maintenance sub-index and lower beef merit.
research institute (Buckley et al., 2000; Snijders et al., The lower BW of the elite cows reflects the overall
2001; Horan et al., 2004) and at the commercial farm selection objective of breeding moderate-sized dairy
level (Evans et al., 2006). The findings support the hy- cows requiring less energy for maintenance, whereby a
potheses of Pryce and Veerkamp (2001) and Veerkamp negative economic weighting (−€1.65 per kg cull cow
et al. (2002) that incorporation of fertility traits into weight) is placed on cow size in the EBI (ICBF, 2017).
genetic selection indexes can lead to improved fertility Selection for smaller cows should result in a smaller
performance. maintenance energy requirement, and thus, any extra
Despite the recent inclusion of reproduction traits feed above that needed for maintenance can be con-
and various fertility indicator traits in selection indices verted to milk or body tissues (VandeHaar et al., 2016).
internationally (Miglior et al., 2017; Cole and Van- It is well established that BCS is a key driver of cow
Raden, 2018), modest improvements have been achieved fertility (Berry et al., 2003; Buckley et al., 2003; Weigel,
(Fleming et al., 2019). Worldwide genetic and pheno- 2006; Cummins et al., 2012b). Heritability estimates for
typic fertility trends vary significantly across countries BCS range from 0.07 to 0.60 (Berry et al., 2008), indi-
(Pryce et al., 2014). While none of the modern selection cating that BCS is under considerable genetic control.
indices used globally are based solely on milk fat and Body condition score can be considered a predictor of
protein production (Lucy, 2019), milk production traits fertility in dairy cattle populations where direct assess-
still typically comprise approximately 50% of the total ment of reproductive fitness is not included in the total
index in many countries, with fertility and survival merit index (Tiezzi et al., 2013). It is likely that the
traits typically comprising less than 30% of the total greater BCS observed in elite cows in the present study
index (Cole and VanRaden, 2018). The findings from is an indirect outcome of the high weighting on fertility
the current study indicate that high weighting on direct within the EBI. Conversely, low emphasis on direct fer-

Figure 2. The mean BCS profile of high Economic Breeding Index (elite) and national average Economic Breeding Index (NA) cows during
the gestation-lactation cycle. Data are presented as LSM, and error bars represent the SEM. Elite cows maintained greater mean BCS (P <
0.001; SEM = 0.16) than NA cows from prepartum to the end of the lactation.

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tility traits within selection indices in many countries have been reported, and BCS has recently been incor-
(Miglior et al., 2012) perhaps limits the opportunity porated as a selection trait in New Zealand represent-
for indirect increases in BCS in these countries. Strong ing 7% of the Breeding Worth index (DairyNZ, 2019).
positive correlations between both genetic (Pryce et al., In the present study, greater EBI resulted in greater
2001; Veerkamp et al., 2001; Berry et al., 2003) and BCS in elite cows at calving and during the breeding
phenotypic (Domecq et al., 1997; Buckley et al., 2003; season, and suggests a genetic disposition to maintain
Zink et al., 2011) BCS and reproductive performance minimum threshold BCS levels for optimum reproduc-

Figure 3. Mean circulating IGF-I and insulin concentrations in high Economic Breeding Index (elite) and national average Economic
Breeding Index (NA) cows from wk −2 to 10 relative to parturition. Plasma IGF-I was greater in elite cows than in NA cows during the sampling
period (P = 0.02). Plasma insulin tended to be greater in elite cows than in NA cows during the sampling period (P = 0.06), and a genetic group
(GG) × time interaction was detected (P = 0.03). All values were back-transformed LSM with 95% CI. †P ≤ 0.01.

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Figure 4. Mean circulating plasma glucose, fatty acids, and BHB concentrations in high Economic Breeding Index (elite) and national aver-
age Economic Breeding Index (NA) cows from wk −2 to 10 relative to parturition. Mean plasma glucose, fatty acids, and BHB were similar in
both genetic groups (GG). Values for fatty acids and BHB are back-transformed LSM with 95% CI.

tive success (Buckley et al., 2003). Holmes (1988) re- genetic index of the cow. Similarly, Buckley (1998) re-
ported that changes in body condition during lactation ported that mid- to late-lactation BCS is influenced by
were influenced by both the BCS at calving and the genetic merit for milk production. Horan et al. (2005)

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observed that a New Zealand strain of HF maintained persistent lactation profile identified by O’Sullivan et
higher BCS than a North American HF strain, which al. (2019b). The observed differences in reproductive
was attributed to the fact that the New Zealand strain performance in the present study support the sugges-
were selected for more modest milk production and tion by O’Sullivan et al. (2019a) that differences in
superior reproductive ability and survival than their prioritization of energy utilization between GG con-
North American counterpart. More recently, Cummins tributed to the greater BCS, and consequently superior
et al. (2012b) and Moore et al. (2014) both reported reproductive performance in elite cows.
that greater genetic merit for fertility traits supports
a greater threshold BCS. Past genetic selection for Energy Metabolites and Metabolic Hormones
increased milk production resulted in greater postpar-
tum adipose tissue mobilization to sustain high milk Greater circulating glucose, IGF-1, and insulin con-
production (Roche et al., 2006; McCarthy et al., 2007b; centrations, and significantly lower BHB concentrations
Lucy et al., 2009), largely due to an inability to achieve during the early lactation period indicate that elite
sufficient energy intake to meet energetic requirements cows were in a more favorable metabolic status com-
for milk production. Moore et al. (2014) reported that pared with NA cows. A positive association between
cows with good genetic merit for fertility traits had circulating glucose during the early postpartum period
greater DMI in early lactation compared with cows and likelihood of conception at first service has been
that had poor genetic merit for fertility traits, support- reported (Green et al., 2012; Garverick et al., 2013;
ing maintenance of greater BCS and milk production. Moore et al., 2014). Circulating glucose concentrations
The significantly higher DMI relative to BW, in addi- during the immediate postpartum period may be a key
tion to a slight reduction in the utilization of energy for indicator of a cow’s adaptive ability to meet the de-
milk production in elite cows reported by O’Sullivan et mands of rising milk production while minimizing BCS
al. (2019a), facilitated more favorable energy balance loss (Moore et al., 2014). The findings of Moore et al.
in elite cows compared with NA, which contributed (2014) indicate that genetic selection for fertility traits
to greater BCS. In addition, a slightly reduced persis- results in more favorable glucose status in early lacta-
tency in late lactation for elite cows was reported by tion, which may represent a key inherent difference be-
O’Sullivan et al. (2019b), likely facilitating the appar- tween cows with good or poor genetic merit for fertility
ent increase in the BCS gain in elite cows during late traits. Similar trends have been observed in the present
lactation. In contrast, NA cows experience a decline in study, although the magnitude of difference observed
BCS after parturition, followed by stable BCS through- was smaller than those observed by Moore et al. (2014).
out mid to late lactation, which may facilitate the more Greater IGF-1 concentrations in elite cows is consistent
with a large body of evidence linking greater IGF-1
concentrations with improved reproductive outcomes
Table 4. The effect of genetic group (GG) of Holstein-Friesian dairy (Taylor et al., 2004; Patton et al., 2007; Cummins et al.,
cow on postpartum luteal activity based on the analysis of milk 2012b). The observed differences in circulating IGF-1
progesterone concentrations1
concentrations in the present study perhaps indicate a
GG genetic effect in the regulation of the somatotropic axis,
similar to that observed by (Cummins et al., 2012a,b).
Item Elite NA SEM P-value
Insulin plays a central role in the metabolism of body
C-LA (d) 24.9 26.8 1.21 0.26 tissues, acting as an indicator of energy status. In the
LP1 (d) 10.6 10.7 0.35 0.85
ILI1 (d) 4.6 4.3 0.22 0.33 present study the difference between GG in concentra-
IOI1 (d) 19.2 19.0 0.38 0.79 tions of glucose, insulin, and IGF-1 are consistent with
LP2 (d) 12.0 12.2 0.30 0.63 the differences previously reported for cows with good
ILI2 (d) 4.8 4.4 0.23 0.30
IOI2 (d) 21.0 20.6 0.37 0.56 versus poor genetic merit for fertility traits (Moore et
LP60d 1.8 1.8 0.06 0.56 al., 2014), and consistent with their interlinking roles
LP1 P4 (ng/mL) 19.4 18.8 0.77 0.63 in the regulation of the reproductive axis (Lucy et al.,
LP2 P4 (ng/mL) 21.8 22.6 0.81 0.49
2014). The tendency for greater insulin concentration
1
Elite = high Economic Breeding Index; NA = national average in elite cows, therefore, may also have had a positive
Economic Breeding Index. C-LA = calving to commencement of luteal
activity (luteal activity; milk progesterone ≥3 ng/mL); LP1 = luteal effect on the regulation of the somatotropic axis. The
phase 1; LP2 = luteal phase 2; IOI1 = inter-ovulatory interval 1; IOI2 concentrations of plasma fatty acids were greater in
= inter-ovulatory interval 2; ILI1 = inter-luteal interval 1; ILI2 = elite cows, which was consistent with the BCS changes
inter-luteal interval 2; LP60d = number of luteal phases in the first 60
d postcalving; LP1 P4 = luteal phase 1 progesterone peak concentra- observed in these animals, particularly the numerically
tion; LP2 P4 = luteal phase 2 progesterone peak concentration. greater BCS loss during the period from calving to AI.

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A similar finding was reported by Coleman et al. (2009) with a shortened interval from calving to conception,
comparing New Zealand versus North American strains increased conception rate, and fewer services per con-
of Holstein-Friesian cows. The elite cows had more BCS ception (Darwash et al., 1997). The interval to first
to lose, therefore exhibiting greater circulating concen- ovulation is largely dependent on the endocrinology of
trations of fatty acids. Body condition score losses from the cow, which in turn is largely determined by energy
calving to AI were within the normal ranges, and did balance postpartum (Lucy, 2019). None of the P4 profile
not exceed previously outlined levels of BCS loss known variables were affected by genetics in the present study.
to hinder subsequent fertility performance (Buckley et Similar findings have also been previously reported
al., 2005; Butler, 2005). Achieving high levels of milk (Pollott and Coffey, 2008; Walsh et al., 2008; Bedere et
production and simultaneously maintaining target BCS al., 2016). The observed interval from calving to C-LA
requires exquisite coordination of energy metabolism was broadly consistent with the values reported for HF
across multiple tissues (Moran et al., 2016). Therefore, cows selected for EBI in the study of Leane (2018), but
the present study confirms that selection for high EBI considerably shorter than the reported intervals from
not only contributes to higher BCS and greater repro- calving to C-LA in the study of Horan et al. (2006).
ductive efficiency, but also conveys a genetic predispo- This may be a reflection of the genetic distance between
sition for favorable metabolic and hormonal status. the cows in the respective studies as result of selection
based on EBI. Although the present study indicates
Ovarian Activity little differences in C-LA and estrous cycle character-
istics between GG, previous studies have shown that
Progesterone profiles are useful for identifying the abnormal ovarian activity is common, with only 60%
interval from calving to C-LA and examining estrous of Holstein cows reported to have normal cyclicity,
cycle characteristics. Ovulation within the first month and the major abnormal cyclicity pattern detected is
postpartum is favorable for reproductive success delayed C-LA (Petersson et al., 2006; Cutullic et al.,
(Galvão et al., 2010). Phenotypically, an early return to 2011). Delayed C-LA has been reported in cows with
cyclic activity in postpartum cows has been associated the greatest EBV for milk yield (Windig et al., 2008;

Figure 5. Survival curves for high Economic Breeding Index (elite) and national average Economic Breeding Index (NA) cows across days
post-first calving during the 4-yr study period. The y-axis represents the overall survival. The x-axis represents the number of days post-first
calving. Log-rank test indicates different survival experiences observed between elite and NA (P < 0.01).

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Bedere et al., 2016). Interestingly, Bedere et al. (2016) pecially in seasonal-calving pasture-based systems. The
suggested that exporting milk with higher fat and pro- present study clearly demonstrates that intensive selec-
tein contents was associated with earlier C-LA. The tion for high EBI can reverse negative fertility trends
high levels of milk constituents reported by O’Sullivan incurred through past decades of selection for milk
et al. (2019a) in both GG and the observed intervals production alone and deliver reproductive performance
from calving to C-LA in the present study indicate that and longevity consistent with industry targets. The
the EBI milk and fertility sub-indices are working in mechanisms driving the differences in fertility include
tandem to generate cows with high milk solids produc- modest differences in metabolic and hormonal profiles
tion and more favorable fertility phenotypes. and markedly greater BCS in elite cows compared with
NA cows. The Next Generation Herd plays an impor-
Survival tant role as a futuristic national herd and industry-wide
point of reference for reproductive performance achiev-
With increased longevity, the mean production of the able through selection for high EBI. Ultimately the
herd increases as a greater proportion of culling deci- present study highlights the potential influence of ge-
sions are based on production, and the proportion of netics to deliver genetic and phenotypic gain by placing
mature cows in the herd is increased (Sewalem et al., appropriate emphasis on traits of economic importance
2008). A dairy heifer will produce approximately 75% within a selection objective.
of a mature cow’s milk yield (Hutchinson et al., 2013).
Therefore, reductions in survivability often result in the
ACKNOWLEDGMENTS
genetic potential for milk production never being fully
realized at farm level (Esslemont et al., 2001). Using
The authors thank the farm staff of the Dairygold
data from commercial dairy farms in Ireland, Evans
Research Farm (Teagasc Animal and Grassland Re-
et al. (2006) reported that only 50% of the potential
search and Innovation Centre, Moorepark, Fermoy,
increase in farm profitability through increased milk
Co. Cork, Ireland) for their care of the experimental
production was realized because of poor reproductive
animals. The authors acknowledge A. F. Parlow of the
performance, highlighting the financial importance of
National Hormone and Peptide Program (NHPP, Tor-
excellent reproductive efficiency. Lopez-Villalobos et
rance, CA) for provision of the IGF-I primary antibody
al. (2000) reported a dual effect of increased survival
(anti-human IGF-I; NHPP167 NIDDK AFP 4892898).
on profitability through lower replacement rates and
We thank John Furlong (School of Veterinary Medi-
greater herd milk yields arising from a higher propor-
cine, University College Dublin, Ireland) for technical
tion of mature animals in a simulation study of sea-
assistance with IGF-I and insulin assays. The authors
sonal calving herds in New Zealand. Similarly, previous
have not stated any conflicts of interest.
economic analyses attributed increased profitability
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