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A New Gene Mapping Resource: Interspecies Hybrids Between Pere David’S Deer (Ehphurms Davidianus) and Red Deer (Cewus Ektphus)

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A New Gene Mapping Resource: Interspecies Hybrids Between Pere David’S Deer (Ehphurms Davidianus) and Red Deer (Cewus Ektphus) Copyright 0 1995 by the Genetics Society of America A New Gene Mapping Resource: Interspecies Hybrids Between Pere David’s Deer (Ehphurms davidianus) and Red Deer (Cewus ektphus) M. L. Tate,* H. C. Mathias,” P. F. Fennessy, K. G. Dodds, J. M. Penty* and D. F. Hill* *AgResearch Molecular Biology Unit, Department of Biochemistry, University of Otago New Zealand and AgResearch, Invermay Apicultural Centre, Mosgiel, New Zealand Manuscript received May 2, 1994 Accepted for publication November 28, 1994 ABSTRACT Three male F1 hybrids between Pere David’s deer and red deer were mated to red deer to produce 143 backcross calves. The pedigrees a are rare exampleof a fertile hybrid between evolutionarily divergent species. We examined the use of these families for genetic mapping of evolutionarily conserved (Type I) loci by testing for genetic linkage between five speciesspecific protein variants 12and conserved DNA probes. Two probes were homologous, and the remainder syntenic, to the protein coding loci in cattle or humans. Using six restriction enzymes, eachDNA probe detected one or more restriction fragments specific to Pere David’s deer. Linkage analyses among the species-specific variants placed the loci into four linkage groups within which linkage between adjacent loci and gene order was supported by a LOD > 3. The linkage groups were( HPX, HBB) -FSHBACPZ, LDHA-W5-IGFZ, BMP3 ( CC, ALB) - ( KIT, PDGFRA) and LDLI”C3-FGFl. Southern and protein analysisof LDHA and ALB provided identical segregation data. These linkage groups were consistent with the cattle gene map and provide new information for comparing the gene maps of ruminants, humans and mice. The deer hybrids are an important new resource that can contribute to the comparative analysisof the mammalian genome. N the 1970s, cytological analyses demonstrated that genes responsible for variation in phenotypic traits. How- I karyotypic banding patterns could be used to align ever, with the exception of the mouse map, veryfew chromosomes and chromosome segments between gen- of the markers on linkage maps are suitable for cross era, families and, in some cases, orders of mammals referencing and alignment of the various mammalian ( SUMNER1990). These data have been extended using genome maps. Typically linkage maps are composed of gene maps that compare the chromosomal location of highly polymorphic microsatellites(WEBER and MAY homologous loci among species (O’BRIENet al. 1985, 1989), which are usually anonymous and, with a few 1988) and such comparisons are most advanced in the notable exceptions (STALLINGet al. 1991 ) , not widely extensively mapped genomes ofmice and humans conserved among mammals. O’BRIENet al. ( 1993) has ( O’BRIEN1991; NADEAUet al. 1993). There is consider- formalized this distinction of marker types, defining the able interest in refining and extending the comparison evolutionarily conserved markers as “Type I” markers of gene maps to a wider variety of speciesin an attempt and the highly polymorphic but anonymous markers as to unify the genetic analysis of mammals and to provide “Type 11” markers. insights into mammalian genome organization and eve Only the mouse has a detailed linkage map of Type I lution (EDWARDS1991; FARRand GOODFELLOW 1992; markers and the key to the production of this map has O’BRIENet al. 1993). been the use of interspecies hybrid backcross mapping Genetic linkage mapping is currently the most produc- pedigrees ( COPELANDandJENKlNS 1991 ) . The principle tive technique in the refinement of gene maps of a wide example is an interspecies hybrid between Mus spetus variety of mammals, such as humans (WEISSENBACHet and M. musculus (the laboratory strain C57BL/ 6J) . al. 1992) , mice ( DIETRICHet al. 1992; COPELANDet al. These and othermouse interspecies hybrids continue to 1993) , rats ( SERIKAWAet al. 1992) , cattle ( BARENDSEet be the method of choice for mapping expressed genes aZ. 1994; BISHOP et al. 1994), sheep ( CRAWFORDet al. and refining the genetic map of the mouse ( COPELAND et al. 1993). The important feature of these interspecies 1994) and pigs ( ELLIGRENet al. 1994). Linkage maps provide the ability to rapidly determine the location and hybrids is that the genetic divergence between the spe- cies is such that species specific variants can be rapidly order of polymorphic genes and the potential to locate identified with virtuallyany DNA geneprobe. Each marker with species specific variants is heterozygous in Corresponding author: Mike Tate, AgResearch Molecular Biology Unit, Biochemistry Department, University of Otago, P.O. Box 56, the F1 hybrid and thus fully informative in backcross Dunedin, New Zealand. E-mail: [email protected] panels. Genetics 139 1383-1391 (March, 1995) 1384 M. L. Tate et al. Conceptually,this approach could beused to effi- gating in the backcross herd ( TATEet al. 1992; EMERSON ciently generate linkage maps of TypeI loci from a wide and TATE1993). We have used the term “variant” for variety of mammalian genera. Parallels havebeen drawn the fixed differences observed between the species and between the mouse hybrids and crosses created for ge- reserved the word “polymorphism” for variation within netic mapping in domestic animals suchas the Bos taurus a species. The five protein variants were assumed to re- X B. indicus hybrid (ROBERTS1990) and crosses among flect variation in the coding gene loci, namely, C3 (com- divergent strains of domestic pig Sus scrofa (ARCHBALD plement component 3), GC ( vitamin D bindingprotein) , ALB et al. 1991) . Although these crossesintroduce some addi- (albumin), LDHA (lactate dehydrogenase A) and HPX tional polymorphism into mapping panels, linkage maps (hemopexin). Loci were chosen for RFLV investigations of Type I markers comparable with those produced with on the basis of homologyor conserved synteny with these M. spetus hybrids (eg: BUCHBERGet al. 1989) have not protein loci in the human and cattle gene maps (Table been forthcoming suggesting these large mammal hy- 1 ) . Three of the proteins, (HPX, LDHA and C3) are brids do not share the wide divergence of the mouse close toproposed evolutionary break points between hu- hybrids. Breeding of wider hybrids for genetic linkage man and cattle chromosomes (O’BRIENet al. 1993) so mapping has been attempted in sheep (sheep X goat we selected gene probes flanking these breakpoints (Ta- hybrids; HILL andBROAD 1991) and cats (Asian leopard ble l ) . X domestic cat; LYONSand O’BRIEN1994) butfew back- cross animals havebeen produced. In marsupials, a sub MATERIALSAND METHODS specificbackcross between tammar wallabiesis being evaluated for linkage mapping ( MCKENZEEet al. 1993). Pedigrees and sampling: Three F1 stags, produced from The interspecies hybrid we have developed is between artificial insemination of red deer hinds with Pere David’s the P6re David’s deer or Milu, Elaphurus davidianus, and deer semen (ASHER et al. 1988; FENNESSY et al. 1991), were mated to red deer from 1989 to 1991 on three New Zealand red deer, Cmus elaphus. The deer species show high deer farms. During this period, the threestags naturally mated level of genetic divergence, similar to that between M. with 91, 21 and 32 red deer, respectively, and semen from spetus and M. musculus ( BONHOMMEet al. 1984). Esti- the lattertwo stags was used to artificially inseminate 31 and 83 mates of the genetic distance (NEI 1972) between the red deer,respectively, using methods described by FENNESSY et deer species are 0.35 from 22 protein loci (EMERSON al. ( 1991 ) . All animals were maintained outdoors onpasture. Blood samples (50- 100 ml ) were taken from all the available and TATE1993) and 0.46 from 45 protein loci (TATEet parents and progeny of these matings. The parents of the al. 1992) . Red deer are the common large deer of Eu- sires had either died soon after mating or were not available rope and closely related subspecies and species are natu- for sampling. However, reference samples were available from rally distributed throughout Europe, Asia and North five P&reDavid’s deer from the grandsires’ herd. America (WHITEHEAD1972). In contrast, P6re David’s Protein variation: Five proteins known to distinguish red deer andP6re David’s deer were scored inthe pedigrees using deer, originally from China, are one of the world’s rarest previously described methods ( TATEet al. 1992; EMERSONand deer species (JONES et al. 1983) . The two species have TATE 1993). Briefly, LDHA was examined by native starch very large differences in their appearance and biology, gel electrophoresis of red blood cell lysates followed by histo- the most notable being the antler, foot and tail morphol- chemical staining. GC, C3 and HPX were analyzed by native ogy ( WEMMER1983), seasonality ( LOUDONet al. 1989), polyacrylamide gel electrophoresis of plasma followed by west- ern analysis using antibodies specific to the human form of disease resistance ( ORRand MACKINTOSH 1988) and be- these proteins (Dako, Carpenteria, CA). ALB was analyzed havior (ALTMANN and SCHEEL1980). However, both by isoelectric focusing at pH 3- 10 with 6 M urea followed by species havethe same number of chromosomes and very general protein staining. similar karyotypes( WANC1988) andfertile hybrids have Selection of DNA probes: Large numbers of cDNA probes from a variety of mammalian sources had been previously occasionally been produced ( BEDFORD1951 ) . Recently, screened for hybridization with red deer DNA on “zooblots,” in New Zealand, Phe David’s deer males that were in which included EcoR1-restricted
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