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Reconstitution and modernization of lost Holstein male lineages using samples from a gene bank

Open ArchivePublished:March 12, 2020DOI:https://doi.org/10.3168/jds.2019-17753

      ABSTRACT

      More than 99% of all known Holstein artificial insemination (AI) bulls in the United States can be traced through their male lineage to just 2 bulls born in the 1950s, and all Holstein bulls can be traced back to 2 bulls born in the late 1800s. As the Y chromosome is passed exclusively from sire to son, this suggests that variation is limited for much of the Y chromosome. Two additional male lineages that are separate from modern lineages before 1890 were present at the start of the AI era and had semen available from the USDA National Animal Germplasm Program (Fort Collins, CO). Semen from representatives of those lineages were used for in vitro embryo production by mating to elite modern genetic females, resulting in the birth of 7 bulls and 8 heifers. Genomic evaluation of the bulls suggested that lineages from the beginning of the AI era could be reconstituted to breed average for total economic merit in 1 generation when mated to elite females due to high genetic merit for fertility, near-average genetic merit for fat and protein yield, and below-average genetic merit for udder and physical conformation. Semen from the bulls is commercially available to facilitate Y chromosome research and efforts to restore lost genetic diversity.

      Key words

      INTRODUCTION

      Rapid genetic change induced by the innovations of AI, breeding value estimation, and genomic selection has enabled substantial increases in milk and component yields (
      • Foote R.H.
      Review: Dairy cattle reproductive physiology research and management—Past progress and future prospects.
      ;
      • García-Ruiz A.
      • Cole J.B.
      • VanRaden P.M.
      • Wiggans G.R.
      • Ruiz-López F.J.
      • Van Tassell C.P.
      Changes in genetic selection differentials and generation intervals in US Holstein dairy cattle as a result of genomic selection.
      ) since 1957. Milk yield for mature Holstein cows has increased by approximately 6,800 L (115% increase); approximately 4,000 L of this increase is due to genetic selection (
      • CDCB (Council on Dairy Cattle Breeding)
      Trend in milk BV for Holstein or Red and White.
      ). With such advances have come various issues for the dairy industry to address, such as declining fertility (
      • VanRaden P.M.
      • Sanders A.H.
      • Tooker M.E.
      • Miller R.H.
      • Norman H.O.
      • Kuhn M.T.
      • Wiggans G.R.
      Development of a national genetic evaluation for cow fertility.
      ), lethal mutations (
      • Cole J.B.
      • Null D.J.
      • VanRaden P.M.
      Phenotypic and genetic effects of recessive haplotypes on yield, longevity, and fertility.
      ), and a loss of diversity within purebred populations (
      • Weigel K.A.
      Controlling inbreeding in modern breeding programs.
      ).
      • Yue X.-P.
      • Dechow C.
      • Liu W.-S.
      A limited number of Y chromosome lineages is present in North American Holsteins.
      reported that 1,821 AI sires were born during the 1960s but that the male lineage of >99% of Holstein AI sires born in 2010 and later could be traced to just 2 of those bulls: Round Oak Rag Apple Elevation (Elevation) and Pawnee Farm Arlinda Chief (Chief). A third bull named Penstate Ivanhoe Star (Ivanhoe Star) was the male lineage ancestor for the remaining <1%, and he and Chief share a common male lineage before 1890.
      The Chief and Ivanhoe Star lines trace their male lineage to Neptune (Holstein Herd-Book registration number 711), who was born in 1883. Elevation's male lineage can be traced to a bull born in 1881 named Hulleman (registration number 886). Two additional male lineages from the start of the AI era were identified by
      • Yue X.-P.
      • Dechow C.
      • Liu W.-S.
      A limited number of Y chromosome lineages is present in North American Holsteins.
      . The first traces to the bull Netherland Prince (registration number 716), who was born in 1880 and has no known male lineage ancestry in common with Neptune or Hulleman. The second lineage traces to Hulleman but splits from the Elevation lineage with a bull named Colantha's 2D Sir Henry (registration number 10497), who was born in 1888. We refer to this second lineage as Colantha.
      Similar to the Holstein breed, male lineages of purebred Jersey cattle can be traced to 1 of 2 sires born in the 1950s who share a common male lineage ancestor that was imported to the United States from the Isle of Jersey (
      • Dechow C.D.
      • Liu W.S.
      • Idun J.S.
      • Maness B.
      Short communication: Two dominant paternal lineages for North American Jersey artificial insemination sires.
      ). Because the Y chromosome is passed exclusively through male lineages, there appears to be few Y chromosome lineages in purebred dairy cattle. Variation in the Y chromosome is an important contributor to male fertility (
      • Yue X.-P.
      • Dechow C.
      • Chang T.-C.
      • DeJarnette J.M.
      • Marshall C.E.
      • Lei C.-Z.
      • Liu W.-S.
      Copy number variations of the extensively amplified Y-linked genes, HSFY and ZNF280BY, in cattle and their association with male reproductive traits in Holstein bulls.
      ), but it is expected that variation in the X-degenerate region of the Y chromosome is limited because of the small number of male lineages (
      • Yue X.-P.
      • Dechow C.
      • Liu W.-S.
      A limited number of Y chromosome lineages is present in North American Holsteins.
      ).
      In addition to the contraction of male lineages, the rate of inbreeding has accelerated in purebred female populations. Inbreeding rates have roughly tripled for Holsteins since the introduction of genomics when comparing current inbreeding rates (0.31% annually from 2013 to 2018) with those of the pre-genomic era (0.10% annually from 2003 to 2008;
      • CDCB (Council on Dairy Cattle Breeding)
      Trend in inbreeding coefficients of cows for Holstein or Red and White.
      ), suggesting a decline in effective population size. Long-term selection limits are tied directly to effective population size (
      • Falconer D.
      • Mackay T.
      Introduction to Quantitative Genetics.
      ), indicating that long-term genetic potential may be compromised due to current high rates of inbreeding. Additionally, breeding objectives change due to shifts in market conditions, regulations, and social concerns. Intensely selected populations with less genetic diversity may be well matched to current conditions but have limited flexibility to adapt (
      • Markert J.A.
      • Champlin D.M.
      • Gutjahr-Gobell R.
      • Grear J.S.
      • Kuhn A.
      • McGreevy T.J.
      • Roth A.
      • Bagley M.J.
      • Nacci D.E.
      Population genetic diversity and fitness in multiple environments.
      ) to changing production conditions and consumer preferences.
      Contraction of animal genetic resources was recognized as a global threat and encouraged the development of conservation programs in the 1990s (
      • Blackburn H.D.
      Development of national animal genetic resource programs.
      ). The National Animal Germplasm Program (NAGP; Fort Collins, CO) was established to address genetic diversity issues confronted by the livestock industry, principally through the development of cryopreserved germplasm collections (
      • Purdy P.H.
      • Wilson C.S.
      • Spiller S.F.
      • Blackburn H.D.
      Biobanking genetic resources: Challenges and implementation at the USDA National Animal Germplasm Program.
      ;
      • Blackburn H.D.
      Biobanking genetic material for agricultural animal species.
      ). The dairy cattle repository of NAGP was facilitated by routine contributions of semen from young bulls by cooperating AI companies, the donation of a historic semen collection by ABS Global (DeForest, WI), and a contribution of semen from the University of Minnesota 1964 control line and other university collections (
      • Hansen L.B.
      Species committee reports: Dairy cattle.
      ). The advent of such programs creates opportunities to characterize genetic resources, reintroduce genetic diversity, and provide a platform for research endeavors. The objectives of this research were to identify additional Holstein Y chromosome lineages within the NAGP semen collection, to introgress the lost Y lineages into a modern autosomal genetic background, and to demonstrate such genetic recovery as a model for other efforts wishing to restore lost genetic diversity.

      MATERIALS AND METHODS

      Male lineages were traced for Holstein bulls in the Council on Dairy Cattle Breeding (Bowie, MD) database that were enrolled with the National Association of Animal Breeders (NAAB; Madison, WI) and that were born in 2010 or later. The lineage of each bull was traced to the earliest known AI sire, and the number of descendants was determined for each male lineage.
      A list of AI bulls that descended from the Netherland Prince and Colantha Holstein Y lineages was obtained (
      • Yue X.-P.
      • Dechow C.
      • Liu W.-S.
      A limited number of Y chromosome lineages is present in North American Holsteins.
      ) and merged with the list of bulls in the NAGP repository. Four sires were matched between the lists for Colantha and 2 for Netherland Prince. Zimmerman Alstar Pilot (Pilot; born Dec. 28, 1954) was the top lifetime net merit ($NM) sire from Netherland Prince's lineage and was selected. One AI sire (Rosafe Caliban) had an official genomic evaluation from the Colantha lineage; however, semen from a son not enrolled in an AI program and born to the University of Minnesota 1964 control line (
      • Boettcher P.J.
      • Hansen L.B.
      • Chester-Jones H.
      • Young C.W.
      Responses of yield and conformation to selection for milk in a designed experiment with a control population.
      ) was selected instead because he had more semen (358 doses) available. That son was U-of-Minn W Caliban Cuthbert (Cuthbert; born Nov. 3, 1989). Although Cuthbert was born in 1989, the University of Minnesota 1964 control line was a nonselected population and his sire was born in 1953, so he represents genetics much older than his birth year.
      Semen from the selected bulls was shipped to TransOva Genetics (Sioux Center, IA) for in vitro embryo production. Oocytes were obtained via ovum pick-up from 3 (July 2016) and 4 (January 2017) elite females owned by Select Sires Inc. (Plain City, OH). Embryos were produced in July 2016 from the Colantha lineage sire and in January 2017 for the Netherland Prince lineage sire. Twelve and 15 embryos from the Colantha and Netherland Prince lineages, respectively, were transferred as fresh embryos into Holstein recipients at the Penn State Dairy Production Research and Teaching Facility (University Park; Penn State Institutional Animal Care and Use Committee protocol no. 47560).
      All males were genotyped for 777K markers with the BovineHD BeadChip (Illumina Inc., San Diego, CA). Four females from the Netherland Prince lineage were genotyped with the BovineHD BeadChip, whereas Colantha lineage females were genotyped with a lower density chip (19K). The bulls were raised at Penn State until approximately 1 yr of age, at which time selected bulls were transferred to a quarantine facility at Select Sires Inc. Semen was collected after release from quarantine in summer 2018 and in winter 2019 from the Colantha and Netherland Prince bulls, respectively.
      Official genomic PTA (gPTA) from April 2019 national genetic evaluations were obtained for Pilot, Cuthbert, their offspring born during the experiment, and the primary active male lineage founders (Chief and Elevation). The gPTA were from the Council on Dairy Cattle Breeding for milk, fat, and protein yields; daughter pregnancy rate (DPR); and $NM. Genomic inbreeding (gF) and genomic future inbreeding (gEFI) were retrieved from the same source. Official evaluations for final type classification score (FS) and udder composite (UC) were obtained from Holstein Association USA Inc. (Brattleboro, VT). The PTA of 1,474 AI bulls that were born in 1965 or earlier and that had at least 50 daughters were likewise obtained. Of those, 56 were genotyped, and only those had evaluations for gF, gEFI, FS, and UC.

      RESULTS

      Lost Lineage Offspring

      Six calves (3 male, 3 female) were born to the Colantha lineage by April 2017, whereas 9 calves (4 male, 5 female) were born to the Netherland Prince lineage by November 2017. At 1 yr of age, the 2 Colantha bulls with the highest gPTA for $NM were enrolled for semen collection at Select Sires Inc. The 3 highest testing Netherland Prince lineage bull calves were also enrolled for semen collection.

      Y Chromosome Lineages

      The Y chromosome lineages for AI bulls born in 2010 and later are shown in Figure 1. In total, 13,316 AI bulls born since 2010 are traced through 7 lineages. Each lineage traces to 1 of 3 original founders (Hulleman, Neptune, and Netherland Price). A straight line represents the most prominent modern lineage, with branches off the main line occurring at the year lineages diverged. For example, the Chief and Ivanhoe Star lineages diverged in 1892, and the Colantha line split from the Elevation lineage in 1888. The earliest AI sire for each lineage was born in the 1950s and is underlined. Chief, Elevation, and Ivanhoe Star are also indicated on their respective lineages to facilitate comparisons with earlier research (
      • Yue X.-P.
      • Dechow C.
      • Liu W.-S.
      A limited number of Y chromosome lineages is present in North American Holsteins.
      ); all 3 are second-generation AI sires and are responsible for all their sire's male lineage descendants. The number of current bulls in the Netherland Prince (3) and Colantha (2) lineages are those bulls generated during this project. The dashed lines in the reconstituted lineages indicate the time between the birth of the bulls born during this project and the last NAAB-enrolled sire of the lineage (Pilot or Rosafe Caliban); Cuthbert is also indicated because he was the sire used to reconstitute the Colantha lineage. The number of current sons in each lineage is indicated on the far right of Figure 1; more than 99% of AI sires born in 2010 and later trace their male lineage through Chief (5,882 descendants) and Elevation (7,412 descendants).
      Figure thumbnail gr1
      Figure 1Current male lineages in the US Holstein population with the first known or founding male ancestor (far left), first National Association of Animal Breeders (NAAB; Madison, WI)-enrolled AI sire of the lineage (underlined), 1960s-era founder of modern lineages (in bold), and number of NAAB-enrolled AI sires born since 2010 (far right). Dashed lines correspond to the 2 reconstituted lineages; the sire used to reconstitute each lineage is italicized.
      Two minor lineages with 1 bull born since 2010 were identified that were not present in a previous analysis of Holstein male lineages (
      • Yue X.-P.
      • Dechow C.
      • Liu W.-S.
      A limited number of Y chromosome lineages is present in North American Holsteins.
      ). Those bulls are specialty sires from high-type classification families and are controlled by a small AI organization (0.22% of AI bulls born since 2010). The sires of the 2 bulls are Hanover-Hill Triple Threat (born in 1972), who is a great-grandson of Lakefield Fond Hope, and Bridon Astro Jet (born in 1978), who is a great-grandson of Ormsby Burke Pontiac Mose. Both Triple Threat and Astro Jet were known as show-type sires.

      Genomic Evaluations

      Genomic evaluations for Pilot, Cuthbert, the dominant AI era male lineage sires (Chief and Elevation), and the average of all AI bulls born before 1965 are reported in Table 1. The values reported in Table 1 are relative to a base of the average Holstein cow born in 2010, so genetic merit for most traits is expected to be negative because of the substantial genetic progress made in the AI era. The active male lineage founders were clearly superior to average bulls from that era for yield traits, udder conformation, and total economic merit ($NM). The average bulls were superior to the active lineage founders for daughter fertility, as indicated by higher DPR. The male lineage founders are more related to the current Holstein population, as indicated by higher gEFI.
      Table 1Genomic evaluations
      Council on Dairy Cattle Breeding (Bowie, MD) and Holstein Association USA Inc. (Brattleboro, VT) genomic PTA from April 2019 for milk, fat, and protein yield; daughter pregnancy rate (DPR); final type classification score (FS); udder composite (UC); lifetime net merit ($NM); genomic inbreeding (gF); and genomic future inbreeding (gEFI).
      for the dominant AI-era male lineage sires and bulls used to reconstitute 2 lost lineages, and the average of all AI bulls born before 1965
      LineageStatusShort nameMilk (kg)Fat (kg)Protein (kg)DPR (%)FSUC$NMgF
      Expressed relative to a 1960 base; can be negative when inbreeding levels were less than the average genotyped animal from that period.
      gEFI
      Expressed relative to a 1960 base; can be negative when inbreeding levels were less than the average genotyped animal from that period.
      NeptuneActiveChief−930−22−300.1−3.65−3.07−6164.16.0
      HullemanActiveElevation−912−29−322.6−2.54−1.76−567−3.36.7
      ColanthaLostCuthbert−1,332−43−365.9−5.21−4.95−7601.81.6
      Netherland PrinceLostPilot−914−16−275.0−6.54−4.33−58110.50.7
      AverageNA
      Not applicable.
      NA−1,398−48−417.2−4.68−4.00−8125.11.9
      1 Council on Dairy Cattle Breeding (Bowie, MD) and Holstein Association USA Inc. (Brattleboro, VT) genomic PTA from April 2019 for milk, fat, and protein yield; daughter pregnancy rate (DPR); final type classification score (FS); udder composite (UC); lifetime net merit ($NM); genomic inbreeding (gF); and genomic future inbreeding (gEFI).
      2 Expressed relative to a 1960 base; can be negative when inbreeding levels were less than the average genotyped animal from that period.
      3 Not applicable.
      Pilot was superior to both of the founding ancestors for component production, superior for daughter fertility, and similar for economic merit. He is also less related (gEFI = 0.7%) to the current Holstein population than the active lineage founders despite being highly inbred himself (gF = 10.5%). Pilot's appeal may have been lessened relative to his contemporaries because his daughters had lower UC and classification scores. Cuthbert was inferior to the founding lineages for most traits except daughter fertility but was higher than the average bulls of the era for yield. He is also less related (gEFI = 1.6%) to the current population than other bulls of the era.
      Average gPTA for yield traits, DPR, FS, UC, $NM, gF, and gEFI of the Cuthbert and Pilot offspring are reported in Table 2. One generation of mating the lost lineage to elite modern genetic females was sufficient to update the lost lineages to near breed average for most traits except FS and UC. For total economic merit, Pilot offspring were slightly above the genetic base of females born in 2010 ($NM = 58.5; range = 5 to 123), whereas Cuthbert daughters were slightly below the base ($NM = −41.5; range = −113 to 22). Offspring from both lineages had very low inbreeding and modest relationships to the current Holstein population. The averages of all NAAB bulls born during 2017 and the top 100 for $NM born during 2017 are also reported for comparison. Although the lost lineage offspring were similar in genetic merit to base-year females, they are inferior to the average of contemporary AI bulls born in 2017.
      Table 2Average genomic evaluations
      Council on Dairy Cattle Breeding (Bowie, MD) and Holstein Association USA Inc. (Brattleboro, VT) genomic PTA from April 2019 for milk, fat, and protein yield; daughter pregnancy rate (DPR); final type classification score (FS); udder composite (UC); lifetime net merit ($NM); genomic inbreeding (gF); and genomic future inbreeding (gEFI).
      of calves sired by Cuthbert (n = 6) and Pilot (n = 8), all NAAB
      National Association of Animal Breeders (Madison, WI).
      -enrolled AI bulls born in 2017 (n = 2,021), and the top 100 lifetime net merit ($) bulls born in 2017
      ItemCuthbertPilotAllTop 100
      Milk (kg)−52.7−52.81,343.11,393.8
      Fat (kg)−2.31.176.8105.8
      Protein (kg)−0.7−1.153.859.9
      DPR (%)0.73.61.41.6
      FS−1.5−2.61.91.5
      UC−1.3−1.22.01.8
      $NM−41.558.5794.5990.8
      gF0.3−0.414.015.8
      gEFI5.55.09.59.4
      1 Council on Dairy Cattle Breeding (Bowie, MD) and Holstein Association USA Inc. (Brattleboro, VT) genomic PTA from April 2019 for milk, fat, and protein yield; daughter pregnancy rate (DPR); final type classification score (FS); udder composite (UC); lifetime net merit ($NM); genomic inbreeding (gF); and genomic future inbreeding (gEFI).
      2 National Association of Animal Breeders (Madison, WI).

      DISCUSSION

      Two Y chromosome lineages have been restored. One of the lineages (Netherland Prince, Figure 2) is separate from all known Holstein male lineages from the time Holsteins were imported into the United States. Netherland Prince was imported as a calf by Smiths and Powell of Syracuse, New York, in October 1880. The second lineage is separate from modern Holstein lineages from 1888 onward.
      Figure thumbnail gr2
      Figure 2Picture of Netherland Prince from the Holstein Herd-Book, Vol. 8, 1885 (
      • Holstein Breeders Association of America
      Holstein Herd-Book.
      ).
      Smaller-scale private-sector companies have also engaged in broadening genetic diversity. Two other 1950s-era male lineages have recently born sons available through AI. Both bulls are niche market sires from show and type classification families; this is similar to the presence of outlier lineages in Jersey cattle (
      • Dechow C.D.
      • Liu W.S.
      • Idun J.S.
      • Maness B.
      Short communication: Two dominant paternal lineages for North American Jersey artificial insemination sires.
      ). Although such sires are not likely to have a widespread influence on their respective breeds in the near future, they do demonstrate that different breeder goals can broaden genetic diversity.
      Identifying sire lines to reconstitute for this project was straightforward because we were targeting very specific sire lineages. The identification of the best lineages may be less straightforward when targeting new traits because individuals in the repository may not have their own or relevant progeny phenotypes. For instance, direct and intentional selection for cow fertility was not practiced in the United States until 2003 (
      • VanRaden P.M.
      • Sanders A.H.
      • Tooker M.E.
      • Miller R.H.
      • Norman H.O.
      • Kuhn M.T.
      • Wiggans G.R.
      Development of a national genetic evaluation for cow fertility.
      ) following a decades-long erosion in genetic and environmental conditions for fertility. Pilot (Table 1) is an example of a bull with a favorable combination of genetic potential for yield and daughter fertility; however, his influence on the current Holstein population is negligible because fertility was not a selection aim during his era. This raises the possibility that the Pilot lineage could have genetic material that is useful for today's population.
      Not all loss of genetic diversity from a selected population is problematic because poor genotypes are removed from the population. Identifying favorable variance from a lineage such as Pilot's that was lost due to a selective sweep as opposed to unfavorable variation lost due to direct selective pressure will require a substantial effort. A large number of daughters from restored lineages would need to be generated to facilitate genomic predictions because a low relationship between a phenotyped and predicted population is associated with lower prediction accuracy (
      • Lee S.H.
      • Clark S.
      • Van Der Werf J.H.J.
      Estimation of genomic prediction accuracy from reference populations with varying degrees of relationship.
      ). That property likely influences the accuracy of the gPTA presented in Table 2 because the modern maternal haplotype may be more accurately represented than the paternal haplotype, which is only distantly related to the current Holstein population.
      Semen from these bulls are now available at the NAGP repository to facilitate expanded research efforts on Y chromosome variation such as runs of homozygosity, admixture, fixation indices, and genetic studies of Y chromosome stability and change. Additional activities are planned to further increase the genetic merit of these Y chromosome lineages by crossing these bulls with elite females. Performance of the daughters from the lost lineages will be evaluated as a model to demonstrate the effects and potential of introgressing long-lost genetic diversity back into a population.
      Clearly, the Holstein population is in a genetic bottleneck in terms of the Y chromosome, and introgression of lost Y chromosomes can add diversity back into the population. A common concern of introgressing dated genetics, in this case over a half century, is lower progeny genetic merit, which will limit their utilization (
      • Leroy G.
      • Danchin-Burge C.
      • Verrier E.
      Impact of the use of cryobank samples in a selected cattle breed: A simulation study.
      ). However, the reported genetic merit of progeny produced in this study suggests that the decrease in genetic merit can be substantially reduced by mating animals of interest to females of high genetic merit with the aid of genomic testing (
      • Gaspa G.
      • Veerkamp R.F.
      • Calus M.P.L.
      • Windig J.J.
      Assessment of genomic selection for introgression of polledness into Holstein Friesian cattle by simulation.
      ). Such animals are still not elite, but potentially mating the progeny to highly targeted cows could result in animals of higher potential. We should be able to evaluate this hypothesis in the next round of planned mating.
      At the time Pilot and Cuthburt samples were obtained, the Holstein Y chromosome issue had not been identified as a potential concern. Therefore, it would seem doubtful that using a targeted collection approach would have been successful in identifying for collection the 2 bulls used. Given our results, it would seem that sampling populations broadly, and perhaps maximizing genetic variability, would be an effective approach for gene banks.
      • Danchin-Burge C.
      • Hiemstra S.J.
      • Blackburn H.
      Ex situ conservation of Holstein-Friesian cattle: Comparing the Dutch, French, and US germplasm collections.
      illustrated how the US Holstein germplasm collection was more diverse than those in France and the Netherlands and more genetically diverse than the 3 countries' in situ populations. Without question, the breadth of the US collection facilitated the introgression of the lost Y chromosomes. Only time will tell whether the collection will have the same utility for yet-unknown issues to emerge.

      CONCLUSIONS

      Two Y chromosome lineages that do not share a common male lineage with active Y chromosome Holstein lineages back to the 1880s have been reconstituted. Introgression of genetic diversity from such lineages into modern Holsteins is a long-term prospect with no guarantee of success; nevertheless, these lines serve as a demonstration of the possibility of using semen from the 1950s to reintroduce lost genetic variation by mating with elite genetic females. The reconstituted lines will facilitate expanded research on Y chromosome variation and function. Semen from the bulls was made commercially available from Select Sires Inc., which will help further evaluation of efforts to reintroduce lost genetic diversity. For this issue, the germplasm collection of the Holstein breed proved capable of providing the genetic diversity necessary and supports broad sampling of in situ populations.

      ACKNOWLEDGMENTS

      The cooperation of many industry partners was essential to this project. Select Sires Inc. (Plain City, OH) is appreciated for supplying donor females and for collecting semen from the respective bulls. Trans Ova Genetics (Sioux Center, IA) is acknowledged for embryo production and transferring the embryos. ABS Global (DeForest, WI) and the University of Minnesota (Minneapolis) are also acknowledged for their semen contributions to the National Animal Germplasm Program (Fort Collins, CO) repository. The staff of the Penn State University Dairy Teaching and Research Center are gratefully acknowledged for their assistance in managing the calves born during the experiment. Funding for the project was provided by USDA (Washington, DC) Cooperative Research Agreement No. 58-5402-4-015. This work was supported by the USDA National Institute of Food and Agriculture (Washington, DC) and Hatch Appropriations under Project No. PEN04691 and Accession No. 1018545. The authors have not stated any conflicts of interest.

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