The Journal of Heredity 2002:93(6)
© 2002 The American Genetic Association 93:429-432
Brief Communication |
A Partial African Ancestry for the Creole Cattle Populations of the Caribbean
From the Department of Genetics, Smurfit Institute, Trinity College, Dublin 2, Ireland (Magee, Meghen, Harrison, Troy, Cymbron, and Bradley); the Institute of Animal Breeding, University of Bern, Bern, Switzerland (Gaillard); the University of Edinburgh, Centre for Tropical Veterinary Medicine, Easter Bush, Roslin, Midlothian, U.K. (Morrow); and CIRAD-EMVT Pathotrop, Campus International de Baillarguet, Montpellier Cedex, France (Maillard).
Address correspondence to D. Bradley at the above address, or e-mail: dbradley{at}tcd.ie.
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Abstract |
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Seventy-eight cattle samples from three Creole Caribbean islands and one Brazilian breed were analyzed for sequence variation in the hypervariable segment of the mitochondrial DNA control region. Seventy-three samples displayed Bos taurus haplotypes, and five samples exhibited haplotypes that were of Bos indicus ancestry. Phylogenetic analysis revealed that all sampled B. taurus sequences fell into two distinct clusters with separate African and European origins. European sequences were encountered in each population; however, the distribution of African haplotypes was uneven, with the highest proportion of African influence found in the Guadeloupe Creole. The reduced levels of African haplotypic variation within the Caribbean and Brazilian are consistent with prior founder effects. Additionally, genetic variation at three microsatellite loci illustrated African influence uniquely in the Guadeloupe Creole. Collectively, the data suggest that this African influence is, at least in part, attributable to the historical importation of African cattle to the Americas. Furthermore, alleles of B. indicus ancestry were detected at appreciable frequencies in all Caribbean Creole populations and may reflect zebu introgressions from either West Africa or the Indian subcontinent.
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Introduction |
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Examination of variation in mitochondrial DNA (mtDNA) control region sequences has been pivotal in the elucidation of bovine phylogeography. Initial studies have demonstrated a deep bifurcation in bovine mtDNA phylogeny, which indicates a predomestic divergence between the two major taxa of cattle, humped zebu (Bos indicus) and humpless taurine (Bos taurus; Loftus et al. 1994). Subsequent genetic investigations have yielded further inference regarding origins within the B. taurus lineage. B. taurus mtDNA sequences fall into one of five ancestral star-like haplotypic clusters, which are geographically distributed (Mannen et al. 1998; Troy et al. 2001). Just one of these clusters, T3, predominates in Western Europe. Symmetrically, diversity within Africa is composed almost exclusively of members of a separate haplotypic cluster, T1, which is rarely detected elsewhere. The almost mutually exclusive geographic distribution of these two haplotypic clusters allows geographical exceptions to be securely identified as secondary introductions, such as the African mtDNA haplotypes encountered in southern Portuguese breeds (Cymbron et al. 1999).
Cattle were first introduced to the Caribbean by Spanish explorers in 1493 (Wilkins 1984), and by 1525 Spanish cattle had spread throughout the Caribbean and much of Central and South America (Felius 1995). Direct shipments of Portuguese cattle to Brazil have also been reported (de Alba 1978; Primo 1992). West African cattle are thought to have entered the continent during the 16th and 18th centuries, presumably as a consequence of slave trade routes, whereas zebu animals were later imported to improve the adaptability of local herds to tropical conditions (Felius 1995; Maillard et al. 1993; Rouse 1973).
To elucidate the genetic ancestry of Creole cattle, we have analyzed molecular diversity in three cattle populations from the Caribbean and one from the South American mainland, using mtDNA sequence and microsatellite allelic variation. The data presented in this study suggest a partial African ancestry for Caribbean Creole populations, the extent of which greatly varies between Caribbean island populations. Although it is probable that a portion of this African genetic contribution originates from the historical African influence associated with the breeds of the Iberian Peninsula, the detection of zebu-specific microsatellite alleles in the modern Caribbean samples suggests some direct importation of West African cattle to the region.
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Materials and Methods |
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Cattle Samples and DNA Extraction
A total of 78 samples from three Caribbean Creole populations—Antigua (21), St. Lucia (13), and Guadeloupe (25)—together with a Brazilian zebu breed, Nelore (19), were analyzed for mtDNA variation. DNA was extracted from blood or serum according to standard protocols previously outlined by Sambrook et al. (1989).
MtDNA Amplification and Sequencing
Molecular diversity was assessed within the most variable 240 base pair (bp) region of the bovine control region (nucleotide positions 16023–16262), which has been widely examined in previous surveys of bovine mtDNA variation (Cymbron et al. 1999; Troy et al. 2001). Partial mitochondrial control regions were amplified, purified, and sequenced with the primers and conditions described by Cymbron et al. (1999). Variations in the control region were identified by direct comparison with the predominant European T3 mtDNA haplotype as previously defined by Troy et al. (2001).
MtDNA-Based Phylogenetic Reconstruction
MtDNA sequences were aligned by eye, and a reduced median network was constructed manually according to the methods outlined by Bandelt et al. (1995). With use of 188 previously published B. taurus mtDNA sequences (Cymbron et al. 1999; Troy et al. 2001), the resulting phylogeny was compared directly to networks constructed for continental European, Iberian, and African populations (Figure 1). The Creole mtDNA sequences reported in this study have been submitted to GenBank.
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Microsatellite Markers and Genotyping
All three Caribbean Creole populations, plus three Portuguese populations, were assayed for allelic length variation at three autosomal microsatellite loci: BM2113 (Sunden et al. 1993), HEL1 (Kaukinen and Varvio 1993), and ILSTS001 (Brezinsky et al. 1992). Microsatellite allele typing was performed according to Loftus et al. (1999). Allele frequencies for each locus were determined by direct counting. The BM2113 and ILSTS001 loci have been described previously as displaying a total of four alleles specific to West African B. taurus breeds, whereas three alleles across the HEL1 and ILSTS001 loci are considered to be exclusive to populations exhibiting B. indicus ancestry (MacHugh et al. 1997). The percentages of both allele groups were averaged to estimate the proportion of West African taurine and zebu admixture for each Caribbean Creole population (Table 1).
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Results |
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MtDNA Control-Region Sequence Variation and Phylogenetic Network Reconstruction
In total, 73 samples displayed B. taurus mtDNA sequences. The remaining five sequences were typical of B. indicus lineages and were detected exclusively in the Nelore breed. Comparison of all Creole B. taurus mtDNA sequences revealed a total of 17 haplotypes, differentiated at 20 polymorphic sites, all of which displayed transitions. This result conforms to the strong transitional bias previously described in the bovine mtDNA control region (Bradley et al. 1996; Cymbron et al. 1999; Loftus et al. 1994; Troy et al. 2001).
Figure 1 places each of the 73 B. taurus Creole sequences in a reduced median network. For comparative purposes, networks were also constructed from previously published Western European, Iberian, and African mtDNA sequences (Cymbron et al. 1999; Troy et al. 2001). Essentially, almost all mtDNA sequences sampled in Europe clustered around the predominant, centrally positioned haplotype T3, through which derivative haplotypes rooted. In Africa mtDNA sequences coalesced to an alternative, predominant variant, T1. The T3 and T1 central variants were separated by three transitions, and the star-like phylogeny of both clusters was consistent with past population expansions, presumably associated with the domestication process (Bradley et al. 1996; Troy et al. 2001). Within Iberia sequences fell into either the European (T3) or African (T1) haplotypic clusters, indicating that these Iberian cattle samples share a partial African ancestry, which is most likely a legacy of historical North African influence in the peninsula (Cymbron et al. 1999).
All Creole B. taurus sequences fell into one of the two distinct European and African continental clusters. Here, the European central mtDNA variant was encountered 16 times, whereas only one sample possessed the central African haplotype. Three additional haplotypes shared all three African T1 haplogroup-defining substitutions, while the remaining 12 haplotypes were typically European. Sequences of European origin revealed patterns of diversity which are consistent with those noted for the European parental population. In contrast, the Creole T1 cluster was atypical of the patterns encountered within the parental African continental population. The most frequently represented African sequence (18 samples) was differentiated from the ancestral T1 haplotype by a total of four nucleotide substitutions and has not been reported in previous surveys of bovine mtDNA phylogeography.
Mitochondrial Admixture Analysis
The proportion of sequences possessing all three T1 haplogroup-defining substitutions were tabulated for each Caribbean Creole population and are presented in Table 1. For B. taurus mtDNA sequence data, the proportion of African mtDNA haplotypes was highest in the Guadeloupe Creole and Nelore populations. Conversely, the incidence of African mtDNA haplotypes in the St. Lucian and Antiguan Creole populations was low.
Microsatellite Allelic Variation and Admixture Analysis
A total of 30 microsatellite alleles were detected in the Caribbean Creole and Iberian samples assayed across all three autosomal microsatellite loci. The mean percentage of West African taurine-specific alleles in three African B. taurus populations was estimated at 39.4%, with low frequencies detected within Iberia. West African taurine-specific alleles were not detected within continental European populations. The Guadeloupe Creole was the only Caribbean population to exhibit West African–specific alleles. B. indicus–specific alleles, the average frequency of which was estimated here as 67.4% in an Indian zebu sample, were also detected at appreciable frequencies within each assayed Caribbean Creole population.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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The data presented in this study suggest a partial African ancestry for the American Creole cattle. MtDNA phylogentic analysis demonstrates that all Creole B. taurus sequences fall into two separate haplotypic clusters, which are representative of European and African continental lineages, as previously described by Troy et al. (2001). The contribution of African mitochondrial sequences to the total B. taurus Creole mtDNA pool is 31.5%, peaking in the Guadeloupe Creole (60.0%) and Brazilian Nelore (42.8%) populations. Conversely, the mtDNA pools of the St. Lucian and Antiguan Creole populations are predominantly European, with African mtDNA admixture proportions of 7.7% and 4.8%, respectively. The Guadeloupe Creole samples also display an average of 6.6% microsatellite alleles that are West African taurine-specific in origin, with no such alleles detected in the Creole populations sampled in St. Lucia and Antigua. Genetic contributions from introgressing zebu cattle are also observed in each of the assayed Caribbean Creole populations, with mean zebu-specific allele frequencies of 22.5% in Guadeloupe, 21.0% in Antigua, and 11.9% in St. Lucia.
B. taurus mtDNA phylogeographic analysis has identified African mtDNA haplotypes in Iberian cattle (Cymbron et al. 1999). Here, 18.3% of the Iberian mtDNA sample was of African origin, while an average of 1.5% of Iberian microsatellite alleles were diagnostic of West African taurine ancestry. It is therefore conceivable that a portion of the African influence noted in Caribbean Creole cattle, particularly that in Guadeloupe, may have originated from either Spanish or Portuguese introductions.
However, two lines of genetic evidence suggest that this African influence is partially attributable to the direct importation of West African cattle to the Caribbean. First, the proportion of African ancestry in the Caribbean Creole cattle, particularly in Guadeloupe, is substantially higher than that reported for the Iberian populations considered in this study. Second, the detection of B. indicus–specific alleles within each Caribbean Creole population, plus the absence of B. indicus mtDNA haplotypes, which is a feature of African zebu populations, suggest West African zebu cattle importations to the region (Hanotte et al. 2002; MacHugh et al. 1997; Maillard et al. 1993).
It is also possible that some of this B. indicus ancestry reflects male-mediated introgression from the Indian subcontinent to the Americas (Felius 1995; Giovambattista et al. 2000; Rouse 1973). Furthermore, the introduction of zebu dams from the Indian subcontinent to Brazil is also supported by the occurrence of five B. indicus mtDNA sequences in the Nelore samples analyzed in this study.
Troy (1998) has demonstrated that approximately five mtDNA haplotypes are encountered in a typical European breed sample size of 12 individuals. A similar value was obtained for the Creole T3 cluster, in which 13 haplotypes were encountered in 50 sequences from one Brazilian and three Caribbean cattle populations. Additionally, the topology of the Creole T3 haplogroup is consistent with that observed for European populations, suggesting that this diversity is a relatively even sample of that encountered within continental Europe. In contrast, the diversity within the Creole T1 haplogroup is markedly different from that found within continental Africa. Here, only four haplotypes were encountered in a total of 23 samples, with a previously undescribed T1 derivative haplotype separated by four substitutions from the T1 central variant, comprising 78.3% of all the African haplotypic variation. Notably, the T1 central haplotype was represented only once. Typically, a continental African breed consisting of 12 samples displays an average of five haplotypes (Troy 1998). This overall reduction in African haplotypic diversity and numerical predominance of a peripheral T1 derivative haplotype within the Creole T1 haplogroup may suggest only a genetic founder effect, in which a restricted subset of the variation within the African parental population has survived and is displayed in modern populations.
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Acknowledgments |
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We thank C. J. Edwards for valuable assistance and discussion. D. A. M. is the recipient of a Trinity College Postgraduate award.
Received January 2, 2002
Accepted November 15, 2002
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References |
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Bandelt HJ, Forster P, Sykes BC, Richards MB, 1995. Mitochondrial portraits of human populations using median networks. Genetics. 141:743-753.[Abstract]
Bradley DG, MacHugh DE, Cunningham P, Loftus RT, 1996. Mitochondrial diversity and the origins of African and European cattle. Proc Natl Acad Sci USA. 93:5131-5135.
Brezinsky L, Kemp SJ, Teale AJ, 1992. ILSTS001: a polymorphic bovine microsatellite. Anim Genet. 23:81.[ISI][Medline]
Cymbron T, Loftus RT, Malheiro MI, Bradley DG, 1999. Mitochondrial sequence variation suggests an African influence in Portuguese cattle. Proc R Soc Lond B Biol Sci. 266:597-603.[Medline]
De Alba J, 1978. Progress in the selection of the Latin American diary Criollo. World Anim Rev FAO. 28:26-30.
Felius M, 1995. Cattle breeds—An encyclopaedia. Doetinchem, the Netherlands: Misset.
Giovambattista G, Ripoli MV, De Luca JC, Mirol PM, Liron JP, Dulout FN, 2000. Male-mediated introgression of Bos indicus genes into Argentine and Bolivian Creole cattle breeds. Anim Genet. 31:302-305.[CrossRef][ISI][Medline]
Hanotte O, Bradley DG, Ochieng JW, Verjee Y, Hill EW, Rege JE, 2002. African pastoralism: genetic imprints of origins and migrations. Science. 296:336-339.
Kaukinen J, Varvio SL, 1993. Eight polymorphic bovine microsatellites. Anim Genet. 24:148.[Medline]
Loftus RT, Ertugrul O, Harba AH, El-Barody MA, MacHugh DE, Park SD, Bradley DG, 1999. A microsatellite survey of cattle from a centre of origin: the Near East. Mol Ecol. 8:2015-2022.[CrossRef][Medline]
Loftus RT, MacHugh DE, Bradley DG, Sharp PM, Cunningham EP, 1994. Evidence for two independent domestications of cattle. Proc Natl Acad Sci USA. 91:2757-2761.
MacHugh DE, Shriver MD, Loftus RT, Cunningham P, Bradley DG, 1997. Microsatellite DNA variation and the evolution, domestication and phylogeography of taurine and zebu cattle (Bos taurus and Bos indicus). Genetics. 146:1071-1086.[Abstract]
Maillard JC, Kemp SJ, Naves M, Palin C, Demangel C, Accipe A, Maillard N, Bensaid A, 1993. An attempt to correlate cattle breed origins and diseases associated with or transmitted by the tick Amblyomma variegatum in the French West Indies. Rev Elev Med Vet Pays Trop. 46:283-290.[Medline]
Mannen H, Tsuji S, Loftus RT, Bradley DG, 1998. Mitochondrial DNA variation and evolution of Japanese black cattle (Bos taurus). Genetics. 150:1169-1175.
Primo AT, 1992. The Iberic cattle in the Americas: 500 years later. Arch Zootec. 41:(suppl.): 421-432.
Rouse JE, 1973. World cattle, III: Cattle of North America. Norman: University of Oklahoma Press.
Sambrook J, Fritsch EF, Maniatis T, 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Sunden SL, Stone RT, Bishop MD, Kappes SM, Keele JW, Beattie CW, 1993. A highly polymorphic bovine microsatellite locus: BM2113. Anim Genet. 24:6.
Troy CS, 1998. Mitochondrial DNA phylogeny and biogeography of domesticated cattle (PhD thesis). University of Dublin, Ireland.
Troy CS, MacHugh DE, Bailey JF, Magee DA, Loftus RT, Cunningham P, Chamberlain AT, Sykes BC, Bradley DG, 2001. Genetic evidence for Near-Eastern origins of European cattle. Nature. 410:1088-1091.[CrossRef][Medline]
Wilkins JV, 1984. Criollo cattle of the Americas. Animal Genetic Resources Information No. 1, FAO, Rome, Italy.
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