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Journal of Animal Science - Animal Genetics

Genetic variation and differentiation in parent-descendant cattle and bison populations123

 

This article in JAS

  1. Vol. 94 No. 11, p. 4491-4497
     
    Received: Mar 16, 2016
    Accepted: Aug 12, 2016
    Published: October 7, 2016


    4 Corresponding author(s): croninm@aol.com
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doi:10.2527/jas.2016-0476
  1. M. A. Cronin 4*5 and
  2. V. L. R. Leesburg
  1. * School of Natural Resources and Agricultural Sciences, Palmer Research Center, University of Alaska, 1509 South Georgeson Road, Palmer 99645
     USDA Agricultural Research Service, Fort Keogh Livestock and Range Research Laboratory, Miles City, MT 59301

Abstract

Genetic variation and differentiation at 32 microsatellite loci was quantified for parent-descendant cattle populations and parent-descendant bison (Bison bison) populations. We compared heterozygosity (Ho) and allelic richness (AR) for 587 cattle of four breeds and three lines derived from them, and 188 bison in three pairs of parent-descendant populations. Ho and AR were less in the Line 1 Hereford inbred cattle population than in the parent Hereford breed. Ho and AR were intermediate in a composite population (CGC, derived from crossing Red Angus, Charolais, and Tarentaise) compared to the three parent breeds. Crossbreeding of Line 1 with CGC resulted in an F1 generation with increased Ho and AR relative to Line 1 and CGC, followed by decreased Ho and AR in 2 backcross generations to Line1. Three transplanted wild bison populations had smaller Ho and AR than their respective parent populations. These data demonstrate that genetic variation reduced from founder effects or inbreeding can be restored with crossbreeding and gene flow.



INTRODUCTION

Quantification of genetic variation and its effect on fitness is integral to cattle research and breeding programs. Genetic issues relevant to bison (Bison bison) management are like those with cattle, including loss of genetic variation and inbreeding in small populations, adaptation to different environments, migration, and introgression resulting from crossbreeding subspecies and species (Hedrick, 2009; Gates et al., 2010). Research on cattle with known ancestry and controlled breeding allows assessment of the nature and extent of changes in genetic variation resulting from inbreeding, crossbreeding, and selection. Examples include three cattle lines at the USDA Fort Keogh Livestock and Range Research Laboratory in Miles City, Montana. The Line 1 Hereford population has been an inbred line since 1934 (MacNeil, 2009). The composite gene combination (CGC) population was created in 1979 by crossing Red Angus, Charolais, and Tarantaise (Newman et al., 1993). A third descendant line, (Red Face, RF), was established in 2000 by crossing Line 1 Hereford bulls and CGC heifers to produce an F1 generation and two generations of backcrossing Line 1 bulls to RF cows (Grosz and MacNeil, 1999).

Wild bison populations have been established with transplants from parent herds in several areas. Three such populations are in the Henry Mountains of Utah established with stock from Yellowstone National Park and two bison populations in Alaska, one established with stock from the National Bison Range in Montana and one with stock from Elk Island National Park in Alberta Canada. Such descendant populations are expected to have less genetic variation than the parent population due to founder effect and genetic drift.

In this study we demonstrated livestock breeding practices that can provide guidance for genetic management of bison and other wildlife. Our objective was to quantify and compare changes in genetic variation at the same loci in parent-descendant cattle and bison populations.


MATERIALS AND METHODS

Animals

The cattle used in this project were kept at the USDA Fort Keogh Livestock and Range Research Laboratory in Miles City, Montana. All procedures involving animals used in this research were approved by the Fort Keogh Animal Care and Use Committee (ACUC # 020104-9). The Line 1 Hereford population has been maintained as an inbred line since 1934 after its creation in a project originally designed to achieve heterosis by crossing selected inbred lines (MacNeil, 2009). Research on Line 1 Herefords has contributed to understanding heritability, genetic correlation, maternal genetic effects, heterosis, and genotype x environment interactions in beef cattle. Germplasm from Line 1 Herefords has been used by Hereford breeders across the U.S. and in other countries (Leesburg, 2012). The Line 1 population at Fort Keogh currently has approximately 200 cows. The composite gene combination (CGC) population was created in 1979 with inter-breed crosses to produce a final composition of 1/2 Red Angus, 1/4 Charolais, and 1/4 Tarentaise (Newman et al., 1993). The CGC population was developed to produce a line of cattle uniquely suited to the cold and dry environment of the U.S. Northern Great Plains. The CGC population at Fort Keogh currently has approximately 560 cows. A third descendant line, called Red Face (RF), was established in 2000 by crossing Line 1 Hereford bulls and CGC heifers to produce an F1 generation followed by two generations of backcrossing Line 1 bulls to RF cows (Grosz and MacNeil, 1999; Tshipuliso et al., 2008). The project succeeded in using marker-assisted selection to introgress the S+ allele at the S-locus (which affects coat color spotting) from CGC into Line 1. This resulted in the RF line without the white face, belly, feet, and tail that are characteristic of Herefords, but with predominantly Line 1 Hereford genetic background. The RF herd had approximately 60 cows when it was dispersed in 2013.

Two bison subspecies are recognized, plains bison (B. b. bison) and wood bison (B. b. athabascae) based on morphology. However, these designations are equivocal because morphological and molecular genetic data suggest that plains bison and wood bison are not differentiated enough to warrant subspecies status (Cronin et al. (2013) and references therein). Wild plains bison populations were created in the Henry Mountains of Utah (HM) with 23 animals transplanted from Yellowstone National Park (YNP) in the 1940s and in Alaska (AKPB) with 22 animals transplanted from the National Bison Range (NBR) in 1928 (Cronin et al., 2013; Ranglack et al., 2015). The AKPB population currently is about 948 animals in four subpopulations and the HM population is currently approximately 350 animals. A captive wood bison population was established in Alaska (AKWB) in 2003–2008 with 66 animals transplanted from Elk Island National Park Alberta, Canada that originated from the population in Wood Buffalo National Park (WBNP, Polzhein et al., 1996; Wilson and Strobeck, 1999). One hundred thirty Alaska wood bison were released in western Alaska as a wild population in 2015.

Genetic analyses

Genotypes for 32 microsatellite loci were obtained for 587 cattle of four breeds and three lines derived from them (Table 1). Genotypes for the same loci were also obtained for 188 bison in six populations, including three pairs of parent-descendant populations. The microsatellite loci (Supplemental Table S1; see online version of journal to access file) and laboratory methods were described by MacNeil et al. (2007). We excluded two of the 34 loci (BM2613, ILSTS059) used by MacNeil et al. (2007) because no data were obtained in the RF cattle for the BM2613 locus and the ILSTS059 locus did not amplify in bison. The genotype data we used were reported previously for the cattle breeds and bison (MacNeil et al., 2007; Cronin et al., 2013) and for the RF F1, B1, and B2 generations (Tshipuliso et al., 2008). Our analysis included genotypes of cattle representative of Line 1 (born 1988–2003), CGC (born 1989–1995), the RF F1, RF B1, and RF B2 generations (born 2000–2007), and the Red Angus, Charolais, Tarentaise, and Hereford breeds. The bison data we analyzed included parent-descendant populations from Yellowstone National Park (YNP)-Henry Mountains (HM), National Bison Range (NBR)-Alaska plains bison (AKPB), and Wood Buffalo National Park (WBNP)-Alaska wood bison (AKWB).


View Full Table | Close Full ViewTable 1.

Average and standard error (SE) values of genetic variation1 in parent-descendant cattle and bison populations

 
Cattle Population type N AR Na Ho
Bison Population type
Hereford Parental Mean 25.72 3.84 4.84 0.58
(SE) (0.12) (0.25) (0.37) (0.04)
Charolais Parental Mean 21.03 4.44 5.75 0.64
(SE) (0.11) (0.24) (0.33) (0.04)
Red Angus Parental Mean 17.78 4.06 4.78 0.61
(SE) (0.07) (0.22) (0.28) (0.04)
Tarentaise Parental Mean 8.88 4.19 4.28 0.67
(SE) (0.06) (0.22) (0.23) (0.04)
Red Face F1 Descendant Mean 178.81 3.94 6.25 0.70
(SE) (0.09) (0.18) (0.48) (0.03)
Red Face B1 Descendant Mean 152.47 3.44 5.59 0.57
(SE) (0.13) (0.15) (0.40) (0.03)
Red Face B2 Descendant Mean 70.91 3.14 4.84 0.54
(SE) (0.05) (0.14) (0.31) (0.04)
CGC Descendant Mean 47.63 4.41 6.47 0.64
(SE) (0.42) (0.25) (0.49) (0.03)
LINE 1 Descendant & Mean 58.41 2.87 3.81 0.46
Parental (SE) (0.14) (0.15) (0.26) (0.03)
Overall Mean Mean 64.63 4.02 5.18 0.60
(SE) (3.40) (0.18) (0.13) (0.01)
Nat. Bison Range Parental Mean 23.78 3.42 3.50 0.43
(SE) (0.17) (0.28) (0.29) (0.05)
AK plains bison Descendant Mean 41.22 3.24 3.56 0.39
(SE) (0.36) (0.26) (0.30) (0.04)
Yellowstone NP Parental Mean 27.72 3.42 3.56 0.42
(SE) (0.16) (0.28) (0.30) (0.05)
Henry Mountains Descendant Mean 28.31 2.73 2.81 0.39
(SE) (0.33) (0.21) (0.22) (0.04)
Wood Buffalo NP Parental Mean 39.03 3.40 3.75 0.42
(SE) (0.28) (0.27) (0.34) (0.04)
AK wood bison Descendant Mean 24.72 2.84 2.91 0.34
(SE) (0.17) (0.23) (0.25) (0.04)
Overall Mean Mean 30.80 3.80 3.35 0.40
(SE) (0.50) (0.31) (0.12) (0.02)
1N = Sample size
Na = Average number of alleles/locus
AR = Allelic richness
Ho = Observed heterozygosity

Observed heterozygosity (Ho, number of heterozygotes/number of individuals for each locus, averaged over all loci) and average number of alleles per locus for each population and Nei (1972) genetic distance (Ds) between populations were calculated with GenALEx 6.5 (Peakall and Smoose, 2012). Allelic richness (AR, the average number of alleles per locus adjusted for sample size, El Mousadik and Petit, 1996) was calculated with FSTAT 2.9.3.2 (Goudet, 1995). Genetic distances were analyzed with MEGA5 (Tamura et al., 2011) to generate a Neighbor-Joining (NJ, Saitou and Nei, 1987) dendrogram. Ho and AR were compared between pairs of populations with t tests of the 32-locus means, and average Ds between parent and descendant populations were compared with Z-tests of the means with unequal sample sizes, with a significance threshold of P < 0.05.


RESULTS AND DISCUSSION

Cattle

Observed heterozygosity (Ho) was greater (P < 0.001) in the parent Hereford breed than in the descendant Line 1 population (Table 1). Ho in the CGC line was intermediate to, but not different (P > 0.36) from, those of its parent breeds (Red Angus, Charolais, and Tarentaise). Ho was less (P < 0.0001) in the inbred Line 1 than in the crossbred CGC. The Line 1 x CGC cross resulted in an RF F1 generation with Ho that was greater (P < 0.02) than in either parent population. Following backcrossing of Line 1 with RF, Ho decreased but remained greater (P < 0.0009) in the RF B1 and B2 generations than in Line 1 (Fig. 1A).

Figure 1.
Figure 1.

Heterozygosity (Ho) and allelic richness (AR) in (A) cattle and (B) bison populations. Note the different scales on the Y-axes. Abbreviations for cattle populations: Line 1 Herefords (Line 1), Composite Gene Combination (CGC), and Red Face (RF); and abbreviations for bison populations: Yellowstone National Park (YNP), Henry Mountains (HM), National Bison Range (NBR), Alaska plains bison (AKPB), Wood Buffalo National Park (WBNP), and Alaska wood bison (AKWB).

 

Allelic richness (AR) values were comparable to those for Ho (Table 1, Fig. 1A) and were less (P < 0.0002) in Line 1 than in Hereford, CGC, RF F1, RF B1, and RF B2, and were not different (P > 0.15) in CGC compared to Charolais or Tarentaise. A difference from the pattern for Ho was that AR was greater (P < 0.002) in CGC than in Red Angus.

Genetic distances derived from allele frequencies (Ds, Table 2) reflect the cattle population histories, with a greater value (P < 0.023) between breeds (average Ds = 0.24 between Hereford, Charolais, Tarentaise, Red Angus) than between parent breeds and descendant lines (average Ds = 0.18 between Hereford-Line 1; Red Angus-CGC; Charolais-CGC; Tarentaise-CGC). Ds between Line 1 and the RF F1, RF B1, and RF B2 generations (average Ds = 0.10) was less (P < 0.0004) than the Ds between CGC and the RF F1, B1, and B2 generations (average Ds = 0.31), reflecting the one-time Line 1 x CGC cross to produce the RF F1 and two backcross generations of RF to Line 1.


View Full Table | Close Full ViewTable 2.

Genetic distances (Ds, Nei 1972) in bison and cattle populations

 
Cattle Hereford Charolais Red Angus Tarentaise RF F1 RF B1 RF B2 CGC LINE1
Bison
Hereford
Charolais 0.209
Red Angus 0.262 0.205
Tarentaise 0.273 0.204 0.292
RF F1 0.087 0.170 0.239 0.235
RF B1 0.122 0.281 0.369 0.359 0.029
RF B2 0.140 0.316 0.411 0.405 0.050 0.017
CGC 0.243 0.139 0.158 0.225 0.200 0.346 0.394
LINE1 0.205 0.416 0.530 0.506 0.122 0.086 0.090 0.445
AKPB NBR YNP HM WBNP AKWB
AKPB
NBR 0.081
YNP 0.047 0.053
HM 0.169 0.078 0.116
WBNP 0.143 0.070 0.092 0.110
AKWB 0.221 0.135 0.151 0.170 0.061

The NJ dendrogram derived from Ds values reflects the breed ancestry of CGC with the parent Red Angus, Charolais, and Tarentaise breeds in the same cluster (Fig. 2). The other major cluster in the NJ dendrogram reflects the Hereford and Line 1 ancestry, and the decreasing genetic distance (i.e., proximity on the NJ dendrogram) of Line 1 and the RF F1, B1, and B2 generations as shown by Tshipuliso et al. (2008) with Bayesian clustering methods.

Figure 2.
Figure 2.

Neighbor-joining (NJ) dendrogram of genetic distances (Ds) between cattle populations and bison populations. Abbreviations for bison populations: Yellowstone National Park (YNP), Henry Mountains (HM), National Bison Range (NBR), Alaska plains bison (AKPB), Wood Buffalo National Park (WBNP), and Alaska wood bison (AKWB).

 

Bison

In each of the three pairs of parent-descendant bison populations Ho was less in the transplanted descendant population than in the parent population (Table 1, Fig. 1B), although the difference was only significant (P < 0.016) between the parent WBNP population and descendant AKWB population. AR was also less in the descendant bison populations than in the parent populations, and the difference was significant (P < 0.002) between the YNP and HM populations and between the WBNP and AKWB populations.

Ds values of bison were not different (P = 0.47) between the parent-descendant populations (average Ds = 0.086) and between the parent populations (average Ds = 0.071 between YNP, NBR, and WBNP, Table 2). However, the genetic distances reflect the ancestry of the parent-descendant WBNP and AKWB populations that occur in the same cluster in the NJ dendrogram (Fig. 2). The relationships of the other bison herds are not as clear, as the parent-descendant NBR-AKPB populations and the parent-descendant YNP- HM populations do not occur in different clusters in the NJ dendrogram.

Our results demonstrate that crossbreeding (i.e., gene flow) can increase genetic variation after it is reduced during population bottlenecks, founder effects, inbreeding, and genetic drift in small populations. Specifically, one generation of crossbreeding of CGC with the inbred Line 1 cattle resulted in an increase in the number of alleles and heterozygosity in the RF F1 generation. Two backcross generations resulted in a decrease of variation from the F1, and also demonstrated the efficacy of marker-assisted introgression of a recessive allele with recovery of a predominantly Line 1 genetic background as indicated by the proximity of the RF B2 generation and Line 1 in Fig. 2 (Grosz and MacNeil, 1999; Tshipuliso et al., 2008).

The example of the RF experiment gives empirical support for management strategies for bison and other wildlife (e.g., Hedrick, 2009; Gates et al., 2010). Bison in the transplanted populations we assessed had less heterozygosity and numbers of alleles compared to the populations of origin. Low genetic variation in a bison population in Texas was associated with negative effects of inbreeding that were overcome by introducing non-related bison stock (Hedrick, 2009). We do not have data regarding fitness and potential inbreeding effects in the bison herds we studied but crossbreeding and gene flow with unrelated stock, as demonstrated with the Line 1, CGC, and RF cattle, can be used to increase genetic variation in bison or other wildlife populations.

 

References

Footnotes



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