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A Second-Generation Genetic Linkage Map of the Baboon (Papio Hamadryas) Genome ⁎ Laura A

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A Second-Generation Genetic Linkage Map of the Baboon (Papio Hamadryas) Genome ⁎ Laura A View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Genomics 88 (2006) 274–281 www.elsevier.com/locate/ygeno A second-generation genetic linkage map of the baboon (Papio hamadryas) genome ⁎ Laura A. Cox , Michael C. Mahaney, John L. VandeBerg, Jeffrey Rogers Department of Genetics and Southwest National Primate Research Center, Southwest Foundation for Biomedical Research, 7620 NW Loop 410, San Antonio, TX 78227, USA Received 17 January 2006; accepted 29 March 2006 Available online 12 May 2006 Abstract Construction of genetic linkage maps for nonhuman primate species provides information and tools that are useful for comparative analysis of chromosome structure and evolution and facilitates comparative analysis of meiotic recombination mechanisms. Most importantly, nonhuman primate genome linkage maps provide the means to conduct whole genome linkage screens for localization and identification of quantitative trait loci that influence phenotypic variation in primate models of common complex human diseases such as atherosclerosis, hypertension, and diabetes. In this study we improved a previously published baboon whole genome linkage map by adding more loci. New loci were added in chromosomal regions that did not have sufficient marker density in the initial map. Relatively low heterozygosity loci from the original map were replaced with higher heterozygosity loci. We report in detail on baboon chromosomes 5, 12, and 18 for which the linkage maps are now substantially improved due to addition of new informative markers. © 2006 Published by Elsevier Inc. Keywords: Baboon; Linkage map; Quantitative trait loci; Nonhuman primate The construction of genetic linkage maps for nonhuman across those species [3,4]. These comparative maps can be primate species provides information and tools that are useful constructed using linkage analysis (e.g., [5]) or through physical for a number of purposes. One application of genetic linkage mapping methods, such as radiation hybrid mapping [6] or BAC mapping data is the comparative analysis of chromosome end sequencing. A number of different strategies, but most structure and evolution. Linkage or recombination-based importantly whole chromosome painting (e.g., [7–9]), have mapping data can also provide insight into differences among been used to demonstrate homologies among chromosomes species in rates of recombination per megabase and thus across a large number of primate species. But chromosome facilitate comparative analysis of the mechanisms of meiotic painting cannot identify differences in the order of specific gene recombination [1,2]. Possibly the most important application for loci located along a set of orthologous chromosomes in various genetic linkage maps of nonhuman primate genomes is in the species. Comparative karyotype or chromosomal banding performance of whole genome linkage screens designed to studies can provide information concerning inversions or locate and identify quantitative trait loci (QTL) that influence translocations that distinguish the chromosomes of nonhuman phenotypic variation in primate models of basic human biology primate species (e.g., [10]), but these approaches lack the or human diseases. resolution of comparative linkage mapping and have not always Whenever a substantial number of homologous genetic produced consistent results (e.g., [11,12]). markers are analyzed and mapped in more than one species, it is Previous studies of baboons (Papio hamadryas) using whole possible to compare locus order and chromosome organization chromosome painting [13] and chromosome banding (e.g., [12,14]) have established homologies between specific chro- mosomes of this Old World monkey and humans. Development ⁎ Corresponding author. of a first-generation genetic linkage map for the baboon genome E-mail address: [email protected] (L.A. Cox). [5] showed that the locations of individual loci within several 0888-7543/$ - see front matter © 2006 Published by Elsevier Inc. doi:10.1016/j.ygeno.2006.03.020 L.A. Cox et al. / Genomics 88 (2006) 274–281 275 baboon chromosomes (i.e., the order and position of particular now have substantially improved linkage maps by adding microsatellite loci) are quite different from the relative new highly informative microsatellite polymorphisms. positions of those loci in humans and were not always concordant with what was predicted based on chromosomal Results banding studies. There are now a number of additional primate species for which large populations of captive animals with The baboon whole genome linkage map: overview known pedigrees are available [e.g., rhesus macaques (Macaca mulatta), African green monkeys (Chlorocebus aethiops), and The current baboon whole genome linkage map is based on pigtailed macaques (M. nemestrina)]. Further work in com- data from 984 pedigreed baboons (649 females and 335 males) parative linkage mapping using these species will lead to a from 11 extended pedigrees. This represents an increase of better understanding of comparative primate chromosome approximately 40% over the number of genotyped animals used structure and evolution and of differential recombination to create the original baboon linkage map [5]. rates among species [1,2,15]. While over 400 “human” microsatellite marker loci have However, the most significant impact of genetic linkage been amplified in baboons, 284 were sufficiently poly- mapping in nonhuman primates has been the use of whole morphic, yielded consistent results, and met our criteria of genome linkage analysis to locate QTL that influence mapping unambiguously to a unique chromosomal location at physiological characteristics known to be risk factors for odds of 1000:1 or 100:1. These polymorphic markers have an common human diseases. Over the past 5 years, the baboon average heterozygosity of 0.74 (range 0.13–0.93), a mean linkage map has been used in studies related to several polymorphic information content of 0.72, and an average common complex human diseases, and many of these studies spacing of 8.9 cM. The mean number of informative meioses have produced significant evidence for the chromosomal per marker is 815 (standard deviation, SD = 217) and the locations in baboons of biomedically significant QTL. mean number of informative meioses with phase known is Kammerer et al. [16] used the initial baboon linkage map 110 (SD = 49). to locate a QTL that influences sodium–lithium countertran- The total mapped genetic length, calculated by summing the sport, a physiological marker of ion transport that is sex-averaged intermarker distances for ordered autosomal loci, associated with hypertension in humans. Martin et al. was 2354 cM. Comparable total genetic length for humans, [17,18] identified QTL that affect individual variation in calculated by summing the sex-averaged intermarker distances endocrine metabolism among baboons, especially variation in for the same subset of microsatellite markers in humans, was serum estrogen levels. Kammerer et al. [19] and Rainwater et 2930 cM. al. [20] reported the mapping of separate QTL involved in the control of serum levels of low-density lipoprotein cholesterol, Improved mapping of PHA12 a major risk factor for human cardiovascular disease. Other QTL related to diabetes [21,22], osteoporosis [23], and other The genetic linkage map for baboon chromosome 12 diseases have also been identified in baboons using the same (PHA12), which is orthologous to the long arm of human linkage map. chromosome 2 (HSA2q), is the map most improved by our One important factor influencing the statistical power of a recent efforts. In the first-generation linkage map for the baboon genetic linkage analysis to identify QTL is the overall density we reported localization of 17 microsatellite marker loci, 15 at of genetic information provided by the polymorphisms that 1000:1 odds and 2 at 100:1 odds, on this chromosome [5].We are mapped along each chromosome. Both the average have now added 13 more microsatellite markers mapped at spacing between polymorphic loci and the heterozygosity of 1000:1 odds, 2 of which were those previously mapped at 100:1 those polymorphisms in the specific animal population under odds (Fig. 1). This 76% increase in the number of marker loci study affect the overall information available in the genome also increased our estimate of the sex-averaged genetic length of scan and thus affect the statistical power of that study to the mapped portion of this chromosome from approximately 88 detect QTL [24,25]. The first-generation linkage map of the to 136 cM. When we consider the 28 markers mapped at 1000:1 baboon genome was sufficiently informative to support whole odds, the new markers decrease the mean intermarker interval genome linkage analyses and produce the results cited above. from 5.9 to 4.9 cM. The number of alleles per microsatellite However, we have continued to improve the baboon linkage marker locus on PHA12 ranges from 4 to 23, with a mean of 11. map by adding more loci. In some cases, we have identified The estimates of heterozygosity for these marker loci range new loci in regions that did not have sufficient marker density from 0.46 to 0.91, with a mean estimate equal to 0.78. Last, the in the initial map. In other cases, new loci with higher newer data reveal a likely complex rearrangement, not seen in individual heterozygosity have been substituted for initial the original map [5], near the q-terminus of PHA12. In this markers that had relatively low heterozygosity in the rearrangement, the order (pter to qter) of the last 3 microsatellite pedigreed baboon population. The current status of the full marker loci mapped on PHA12 is D2S2176, D2S2338, and baboon linkage map, as well as additional information about D2S206, while their order on HSA2q is D2S206, D2S2176, and specific loci, is available online through the Southwest D2S2338. The maximum likelihood of the “rearranged” baboon National Primate Research Center (http://www.snprc.org). order for these markers is significantly greater than that for the We report here on three baboon chromosomes for which we human order (p = 4.849 × 10−12).
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