Introgressive hybridization and nonconcordant evolutionary history of maternal and paternal lineages in North American deer.
Information from morphology and allozymes suggests that hybridization between white-tailed deer and mule deer occurs in western Texas (Carr et al. 1986; Ballinger et al. 1992). Hybrid zones studies suggest that hybrids are not always readily identified using morphological characters alone (Cronin et al. 1988; Ballinger et al. 1992), although Derr et al. (1991) reported intermediate morphological characteristics for a single first generation hybrid produced in captivity. A potential reason for this is given in Ballinger et al. (1992) which suggests that hybrids in the western Texas zone of contact are primarily backcross individuals. It appears that multiple generations are involved as evidenced by animals which are morphologically identifiable as mule deer yet which possess the homozygous condition for the albumin allele considered to be diagnostic for white-tailed deer. Thus, it appears that morphological characters are inefficient indicators of the existence and precise ancestry of hybrid individuals.
With regard to systematic relationships, analysis of mtDNA variation in Odocoileus gives a pattern distinct from the traditional taxonomy based on morphology. If the species of Odocoileus are defined using maternally inherited mtDNA as the criterion, the mule deer and white-tailed deer would be considered one species and the black-tailed deer would form a second species. Of the six of nine currently recognized subspecies of mule deer for which mtDNA data exists, none appear to have originated from a black-tailed deer ancestor (Carr et al. 1986; Cronin et al. 1988; Ballinger et al. 1992). Perhaps this can be explained by lineage sorting (Avise and Ball 1990) or the capture of mtDNA via preferential dispersal of male deer across a moving zone of hybridization as alluded to by Carr et al. (1986). Regardless of the mechanism, the distribution of mtDNA haplotypes is in conflict with the patterns found in morphological characters and allozymes.
The Y-linked zinc finger gene (Zfy) holds promise for evolutionary and population genetic studies. Examination of this Y-chromosome marker might determine if a paternally inherited element is concordant with patterns seen with biparentally inherited nuclear genes, as has been shown for Mus using the Sry system (Tucker et al. 1992; Lundrigan and Tucker, 1994), or with the phylogenetic patterns derived from maternally inherited mtDNA. The objective of this study is to use a paternally inherited Zfy marker to examine the direction and scope of hybridization between mule deer and white-tailed deer in western Texas.
MATERIALS AND METHODS
Samples were collected from male deer from throughout the United Sates (Table 1). Emphasis was placed on documented areas of hybridization (Carr et al. 1986; Ballinger et al. 1992), including samples from 26 deer from within the zone of sympatry in western Texas. based on morphological criteria, nine of the western Texas males were considered white-tailed deer and 17 were considered mule deer. None of these animals appeared to be hybrids based on morphology. Two additional animals came from the zone of sympatry outside of western Texas, including one mule deer from Utah, and one white-tailed deer from Arizona. These 28 animals all conformed to the morphological criteria for their respective species. An additional 14 white-tailed deer, one mule deer, and four black-tailed deer were examined from outside the region of overlap between species.
Amplification and Band Excision
Genomic DNA of deer was extracted using standard phenol/chloroform procedures (Maniatis et al. 1982) from heart, liver, or kidney tissues that were stored at -80 [degrees] C. The polymerase chain reaction (PCR; Saiki et al. 1988) was employed to enzymatically amplify DNA sequences (800-900 bp) within the Zfx and Zfy genes. Amplified products from LGL-331 (5[prime]-CAA-ATC-ATG-CAA-GGA-TAG-AC-3[prime]) and LGL-335 (5[prime]-AGA-CCT-GAT-TCC-AGA-CAG-TAC-CA-3[prime]) were electrophoretically separated in a 2.2% low-melting agarose gel. Females showed a single-band pattern from the PCR amplification; whereas males typically showed a two-band pattern because the Zfx intron was slightly larger than the Zfy intron. We isolated the smaller Zfy product by using a Pasteur pipette to band-punch a core sample from the low-melting agarose gel. The core sample was reconstituted with 100 [Mu]l of d[H.sub.2]0, and two microliters of this solution were used in a second amplification.
Sequencing and RFLP Analysis
The Zfy intron from three male specimens (white-tailed deer [BGH-1], mule deer [UTAH-2], and black-tailed deer [ALA BT 35]) and the Zfx from three female specimens (white-tailed deer [OV 3804], mule deer [AK 7975cb, and Alaska black-tailed deer ) were sequenced by using the ABI PRISM Terminator Cycle Sequencing Ready Reaction Kit (Carr and Marshall 1991) using the LGL-331 and LGL335 primers. These extensions each provided over 400 bp of single-strand sequence for the amplified Zfx gene or band extracted Zfy gene fragment. Sequence alignments were made using the computer software package SeqEd (Applied Biosystems Inc., Foster City, California). based on these sequence alignments, two internal primers were developed (LGL-331Y 5[prime]-GAA-ACC-CAA-TTA-AAA-TAT-ATG-AAGCA-3[prime] and LGL-335Y 5[prime]-GAA-GCA-A/GGC-ACA-TTC-ATA-GAG-GA-3[prime]).
Primers LGL-331/LGL-335Y and LGL-331Y/LGL-335 were used as the amplification and sequencing primers to analyze the Y-specific fragment. Complete double strand sequences for the final intron of Zfy was produced for one white-tailed deer (11 pt WT), one mule deer (Cal 2 MD) and one black-tailed deer (ALAS 48), one caribou, and one moose. Sequences were obtained by using an ABI PRISM 310 and ABI 373A automated DNA sequencer (Applied BioSystems Inc.). Sequences were aligned using the computer package Sequencher 3.0 (Gene Code Corporation, Ann Arbor, Michigan).
Analysis of sequence data revealed the presence of a diagnostic MseI site which differentiated the O. hemionus samples from the O. virginianus samples. The remaining animals were screened for variation at the MseI site by restriction fragment length polymorphism (RFLP) analysis. Prior to the development and implementation of the LGL-335Y primer as an amplification primer, all Zfy products were generated for RFLP analysis by band excision. After the development of LGL-335Y, Zfy-specific fragments were directly amplified and cut with MseI. In all cases where we have done side-by-side comparisons both techniques have given wholly equivalent results.
Double stranded sequence data for the five animals which were analyzed using the program Phylogenetic Analysis Using Parsimony 3.1.1 (PAUP 3.1.1) to reconstruct the phylogeny of the Zfy gene for Odocoileus. The Zfy of the genera Alces and Rangifer were sequenced to generate data for outgroup comparison. We used the percent divergence generated by PAUP to develop a phenogram depicting the level of divergence of the Zfy intron to compare with the percent divergence data for mtDNA previously reported by Carr et al. (1986). PAUP 4.0(*) was used in an attempt to test for data incongruity between the mtDNA data of Carr and Hughes (1993) and the Zfy data discussed herein.
The amplification and sequence results of the five taxa produced an 881-bp alignment of the Zfy intron for a male white-tailed deer, mule deer, black-tailed deer, caribou, and a moose using LGL-331/335Y and LGL-331Y/335. The three Odocoileus taxa were found to have nine variable nucleotide positions. The white-tailed deer had a total of eight nucleotide changes which distinguished its Zfy from that found in mule deer and black-tailed deer. A single site changed was found to distinguish the California mule deer from the sitka black-tailed deer. Although mule deer and black-tailed deer differed by a single nucleotide no restriction endonuclease was found which recognized this variable site.
Forty-nine deer from 11 localities were assayed via restriction endonuclease analysis for the variable MseI site. This sample included nine white-tailed deer and 17 mule deer that were collected in the west Texas hybrid zone. Additionally. 15 white-tailed deer, two mule deer, and two black-tailed deer from outside of the contact zone and a pen-raised [F.sub.1] hybrid were also included in the analysis. All animals outside the western Texas contact zone had the MseI RFLP pattern that corresponded correctly to the Zfy restriction phenotype suggested by sequence analysis of the respective taxa. Animals collected within the contact zone were identified to species by morphology, including antler morphology and length of the metatarsal gland.
Two of the 27 animals from the contact zone had Zfy restriction phenotypes not characteristic of the species to which they were identified (Table 1). Both possessed mule deer morphology, but the RFLP marker was that of white-tailed deer To insure reliability, a captive-bred F.sub.1] hybrid was included in the analysis. This individual was the offspring of a female mule deer O. hemionus crooki and a male white-tailed deer O. virginianus texanus (Derr et al. 1991). As expected this individual had the white-tailed deer Zfy restriction pattern.
The pattern of mtDNA divergence among populations of white-tailed deer, black-tailed deer, and mule deer is inconsistent with their current taxonomic relationships as suggested by morphological datasets. High mtDNA sequence divergence (6-7%) has been reported between mule deer (O. crooki and O. h. hemionus) and its conspecific black-tailed deer (0. h. sitkensis and O. h. columbianus). White-tailed deer and mule deer exhibited low (0-2%) mtDNA sequence divergence (Carr et al. 1986, Cronin et al. 1988, Derr 1990). This paradox between traditional taxonomy and mtDNA was hypothesized to be either the result of introgression of mtDNA from white-tailed deer into mule deer populations (Carr et al. 1986) or the phylogenetic sorting of shared mtDNAs when mule deer and black-tailed deer were isolated during the Pleistocene (Cronin et al. 1988). In order to determine if the unexpected relationship between white-tailed and mule deer was characteristic of paternal lineages as well, sequence and RFLP analyses of a Y-linked gene (zinc finger Y-Zfy) were performed.
Paternal Gene Flow
Analysis of the RFLPs for the Zfy nuclear locus supports recent hybridization between these two species. Two of the 26 individuals collected from within the western Texas contact zone were identified as hybrids by this marker Allozyme data for the diagnostic albumin locus, which we were able to obtain from earlier studies, confirmed these animals as hybrids. Although both had mule deer morphology, one was homozygous for the white-tailed deer albumin allele (JND-8423) and the other (JND-8433) was heterozygous (Ballinger et al. 1992). This demonstrates that the white-tailed deer Zfy lineage has persisted through at least two generations in the mule deer population in both respective lineages. The combination of mtDNA, allozymes, and Zfy datasets clearly serve to provide more resolution regarding the direction of gene flow between deer populations.
Haldane's Rule, mtDNA Capture, and Hybridization in Odocoileus
The white-tailed deer/mule deer contact zone in western Texas is irregular and mosaic in nature. Its borders are not easily defined as in most other hybrid zones where abrupt clines delineate species' boundaries. Traditionally, hybrid zones have been described along linear transects (Barton and Hewitt 1981, 1985) where prominent differences are notable among species. Because of its mosaic nature, Derr (1990) suggested that shifting environmental conditions have played a large role in demarcating areas of hybridization in the TransPecos region of Texas. Normally, white-tailed deer inhabit more mesic, riparian zones, whereas mule deer occur in drier, upland areas (Mackie 1981; Gavin and May 1988). In western Texas, white-tailed deer have encroached into the range of mule deer as the succession of woody vegetation communities has increased (Wiggers and Beasom 1986), thus increasing the opportunity for interspecific interactions and subsequent mating events.
Cronin (1991) suggested that the direction of hybridization could be the result of habitat choice of the [F.sub.1] hybrid offspring. This hypothesis could explain the presence of shared albumin alleles between these species within the contact zone where gene flow is not unidirectional. Carr et al. (1986) reported that interspecific matings most likely occurred between mule deer males and white-tailed deer females with the [F.sub.1] hybrids being incorporated into the mule deer population. based on restriction mapping of mtDNA these authors reasoned that such matings resulted in the introgression of white-tailed deer mtDNA into the mule deer gene pool through the mating of white-tailed does and mule deer bucks. Ballinger et al. (1992) analyzed mtDNA restriction sites and allozymes of mule deer and white-tailed deer from western Texas and found an mtDNA genotype that was shared by 67% of the white-tailed deer and 100% of the mule deer. However, Carr and Hughes (1993) have now shown that their sequence data for their WTX haplotype (equivalent in part to the LoA restriction haplotype of Carr et al.  as discussed by Carr and Hughes ) is most parsimoniously interpreted to mean that the common mtDNA haplotype found in both mule deer and white-tailed deer in the area of the Longfellow Ranch in western Texas was of mule deer origin. If this is true, the data support the contention that the predominant successful breeding is between white-tailed bucks and mule deer does, which is the opposite direction of hybridization suggested by Carr et al. (1986).
Further support for this hypothesis comes from the allozyme data for the albumin locus for deer in the Longfellow Ranch portion of the western Texas hybrid zone (Ballinger et al. 1992). Twenty-four percent of the mule deer examined were heterozygous for an allele that is diagnostic for allopatric white-tailed deer Among the 46 animals morphologically identified as mule deer, 6.5% of these deer were homozygous for the otherwise diagnostic white-tailed deer allele. Therefore, the level of hybridization on the Longfellow Ranch mule deer population appears to have gene frequencies above what would be expected of an F2 hybrid population. Conversely, 12.5% of the 24 white-tailed deer were heterozygous for the mule deer allele with none being homozygous for this allele. These data clearly suggest the predominant movement of genes is from the white-tailed deer population into the mule deer population. In short, the mtDNA data and the albumin data appear to best support male white-tailed deer hybridizing with mule deer does and the white-tailed deer population ultimately capturing the mule deer mtDNA as the white-tailed deer population moves into the previous range of the mule deer This follows the pattern of population movement documented through ecological studies in western Texas (Wiggers and Beasom 1986).
Haldane's rule, which explains why [F.sub.1] males are functionally sterile, has been invoked as a primary mechanism in mtDNA capture. Perhaps the best example of this is in Clethrionomys in Scandinavia where mtDNA capture was found between two species that produce sterile [F.sub.1] males (Tegelstrom 1987; Tegelstrom et al. 1988). Our data do not appear to support mtDNA capture due to Haldane's rule as described in Clethrionomys (Tegelstrom 1987; Tegelstrom et al. 1988; Avise 1994). These data appear more reflective of the zone of hybridization for Mus musculus and M. domesticus in Europe, where backcrossing appears relatively extensive for hybrids of both sexes (for review see Avise 1994). The persistence of the white-tailed deer Zfy among wild backcrossed mule deer hybrids clearly indicates [F.sub.1] male fertility as was observed in the captive bred [F.sub.1] (Derr et al. 1991). This is a critical observation as it shows that observations involving male hybrids are not necessarily biased by artificial survivorship of these hybrids in captive situations. Therefore, the extensive mtDNA capture seen in O. virginianus and O. hemionus cannot be explained as a simple consequence of Haldane's Rule.
Mitochondrial DNA and Zfy
The pattern of divergence of Zfy indicates that conspecific mule deer and black-tailed deer are more closely related to each other than either is to white-tailed deer [ILLUSTRATION FOR FIGURE 1 OMITTED]. This is consistent with the traditional taxonomic arrangement but differs from the relationships determined by mtDNA studies. We have tried to test these data for incongruence using PAUP 4.0(*). Unfortunately, the number of characters for the available mtDNA sequences and for our Zfy sequences do not include enough variable characters to allow a meaningful analysis within the power of this test. Therefore, while the Zfy sequences are consistent with the present taxonomic relationships based upon morphology and allozymes, we cannot currently show these datasets to be incongruent with the mitochondrial data with statistical certainty. Although the current sequence datasets are not large enough to allow tests of incongruence between the Zfy and mtDNA data, it is appropriate to make the following points. Data presented in Cronin (1992) were shown to differentiate the Alaska, British Columbia, and Oregon black-tailed deer mtDNA haplotypes from the mule deer and western white-tailed deer haplotypes by 25 restriction site changes, whereas the greatest number of restriction site changes within the clade which included western white-tailed deer and mule deer was six restriction site changes. To date no author who has studied the evolution of mtDNA in the Odocoileus-complex has suggested that mule deer and white-tailed deer mtDNA haplotypes were clearly not more closely related to each other than either taxon's mtDNA haplotype was to the typical black-tailed deer mtDNA haplotype, regardless of the type of analysis (sequence or restriction site) or the region on the mtDNA examined. Bootstrap analyses of the data from the Zfy intron give consistent values of 90-95% support for the placement of the black-tailed deer and mule deer as sister taxa relative to the white-tailed deer depending on which cervids are chosen as the outgroup taxa.
Data from the region of the Zfy gene which we have studied has proven to possess sufficient variation to clearly differentiate between O. virginianus and O. hemionus. In addition, sequence variation has been found within O. hemionus. Analysis of the distribution of variation in the Y chromosome in a hybrid zone in west Texas shows that male white-tail deer disperse into the range of mule deer and successfully breed mule deer does. While the resulting [F.sub.1] hybrids are rare, the hybrid population has a high proportion of hybrid animals which must be the result of backcrossing. Carr and Hughes (1993) found that mtDNAs of all mule deer and white-tailed deer they studied showed 1% divergence except in the area of hybridization in west Texas. In this hybrid zone a mtDNA haplotype was described (their WTX) that appears to have originated in the mule deer, but is now shared by both species in the region of the Longfellow Ranch in west Texas. As we have shown that the backcrosses include fertile males, these data do not support Haldane's Rule as a simple explanation of mtDNA capture by the white-tailed deer.
We thank the Texas Co-operative Wildlife Collection, D. Ellsworth, M. Cronin, J. Derr, and S. Sibert for providing deer tissues used in this study. We thank R. Stewart for providing technical assistance. Special thanks are given to R. Baker for critical review of this manuscript and allowing the use of his laboratories and supplies to complete a portion of the study. We are grateful to R. Bradley, A. DeWoody and R. Honeycutt for their comments on an earlier version of this manuscript. This research was funded through a Texas A&M University minigrant and LGL Ecological Genetics, Inc. This manuscript represents contribution number 11 of the Center for Biosystemantics and Biodiversity, Texas A&M University.
ALBERTS, B., D. BRAY, J. LEWIS, M. RAFF, K. ROBERTS, AND J. D. WATSON. 1983. Molecular biology of the cell. Garland Publishing, New York.
AVISE, J. C. 1994. Molecular markers, natural history and evolution. Chapman and Hall, New York.
AVISE, J. C., AND R. M. BALL, JR. 1990. Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surv. Evol. Biol. 7:45-67.
BACCUS, R., N. RYMAN, M. H. SMITH, C. REUTERWAL, AND D. G. CAMERON. 1983. Genetic variability and differentiation of large grazing mammals. J. Mammal. 64:109-120.
BAKER, R. H. 1984. Origin, classification and distribution. Pp. 118 in L. K. Halls, ed. White-tailed deer: ecology and management. Stackpole Books, Harrisburg, PA.
BALLINGER, S. W., L. H. BLANKENSHIP, J. W. BICKHAM, AND S. M. CARR. 1992. Allozyme and mitochondrial DNA analysis of a hybrid zone between white-tailed deer and mule deer (Odocoileus) in west Texas. Biochem. Genet. 30:1-11.
BARTON, N. H., AND G. M. HEWITT. 1981. Hybrid zones and speciation. Pp. 109-145 in W. R. Atchley and D. S. Woodruff, eds. Evolution and speciation: essays in honour of M. J. D. White. Cambridge Univ. Press, Cambridge, U.K.
-----. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113-148.
BULL, J. J., D. M. HILLIS, AND S. O'STEEN. 1988. Mammalian Zfy sequences exist in reptiles, regardless of sex-determining mechanism. Science 242:567-569.
CARR, S. M., S. W. BALLINGER, J. N. DERR, L. H. BLANKENSHIP, AND J. W. BICKHAM. 1986. Mitochondrial DNA analysis of hybridization between sympatric white-tailed deer and mule deer in west Texas. Proc. Natl. Acad. Sci. USA 83:9576-9580.
CARR, S. M., AND H. D. MARSHAL. 1991. Detection of intraspecific DNA sequence variation in the mitochondrial cytochrome b gene of Atlantic cod (Gadus morhua) by the polymerase chain reaction. Can. J. Fish. Aquat. Sci. 48:48-52.
CARR, S. M., AND G. A. HUGHES. 1993. Direction of introgressive hybridization between species of North American deer (Odocoileus) as inferred from mitochondrial-cytochrome-b sequences. J. Mammal. 74:331-342.
CRONIN, M. A. 1991. Mitochondrial and nuclear genetic relationships of deer (Odocoileus spp.) in western North America. Can. J. Zool. 69:1270-1279.
CRONIN, M. A., E. R. VYSE, AND D. G. CAMERON. 1988. Genetic relationships between mule deer and white-tailed deer in Montana. J. Wildl. Manage. 52:320-328.
DAY, G. I. 1980. Characteristics and measurements of captive hybrid deer in Arizona. Southwest. Nat. 25:434-438.
DERR, J. N. 1990. Genetic interactions between two species of North American deer, Odocoileus virginianus and Odocoileus hemionus. Ph.D. dins., Texas A&M University, College Station, TX.
DERR, J. N., D. W. HALE, D. L. ELLSWORTH, AND J. W. BICKHAM. 1991. Fertility in an [F.sub.1] male hybrid of white-tailed deer (Odocoileus virginianus) x mule deer (O. hemionus). J. Reprod. Fertil. 93:111-117.
GAVIN, T A., AND B. MAY. 1988. Taxonomic status and genetic purity of Columbian white-tailed deer J. Wildl. Manage. 52:110.
GEIST, V. 1981. Behavior: adaptive strategies in mule deer Pp. 157-223 in O. C. Wallmo, ed. Mule and black-tailed deer of North America. Univ. of Nebraska Press, Lincoln, NE.
HALL, E. R. 1981. The mammals of North America. 2d ed. Vol. II. Wiley, New York.
LANEEAR, J., AND P. W. H. HOLLAND. 1991. The molecular evolution of ZFY-related genes in birds and mammals. J. Mol. Evol. 32: 310-315.
LUNDRIGUN, B. L., AND P. K. TUCKER. 1994. Tracing paternal ancestry in mice, using the Y-linked, sex-determining locus, Sty. Mol. Biol. Evol. 11:483-492.
MACKIE, R. J. 1981. Interspecific relationships. Pp. 487-507 in O. C. Wallmo, ed. Mule and black-tailed deer of North America. Univ. of Nebraska Press, Lincoln, NE.
MANIATIS, T., E. F. FRITSCH, AND J. SAMBROOK. 1982. Molecular cloning: laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
MARDON, G., AND D. C. PAGE. 1989. The sex-determining region of the mouse Y chromosome encodes a protein with a highly acid domain and 13 zinc fingers. Cell 56:765-770.
MCCLYMONT, R. A., M. FENTON, AND J. R. THOMPSON. 1982. Identification of cervid tissues and hybridization of serum albumin. J. Wildl. Manage. 46:540-544.
MIYATA, T, H. HAYASHIDA, K. KUMA, AND T YASUNAGA. 1987a. Male-driven molecular evolution demonstrated by different rates of silent substitutions between autosome-and sex chromosome-linked genes. Proc. Jpn. Acad. 63(B):327-334.
-----. 1987b. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harbor Symposium, Quant. Biol. 52:863-867.
NICHOLS, R., AND J. MURREY. 1973. Black-tailed deer-white-tailed deer breeding study. Final Report, P-R project W-46 (U-A, VB). Tennessee Game and Fish Commission, Nashville, TN.
PAGE, D.C., R. MOSHER, E. M. SIMPSON, E. M. C. FISHER, G. MARDON, J. POLLACK, B. MCGILLIVRAY, A. BE LA CHAPELLE, AND L. G. BROWN. 1987. The sex-determining region of the human Y chromosome encodes a finger protein. Cell 51:1091-1104.
PALMER, M. S., A. H. SINCLAIR, P. BERTA, N. A. ELLIS, AND P. N. GOODFELLOW. 1989. Genetic evidence that ZFY is not the testis-determining factor Nature 342:937-939.
PAMILO, P., AND N. O. BIANCHI. 1993. Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. J. Mol. Biol. Evol. 10:271-281.
PAMILO, P., AND M. NEI. 1988. Relationships between gene trees and species trees. J. Mol. Biol. Evol. 5:568-583.
SAIKI, R. K., D. H. GELFUND, S. STOFFEL, S. J. SCHARF, R. HIGNCHI, G. T. HORN, K. B. MULLIS, AND H. A. ERLICH. 1988. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487-491.
SINCLAIR, A. H., J. W. FOSTER, J. A. SPENCER, D .C. PAGE, M. PALMER, P. N. GOODFELLOW, AND J. A. M. GRAVES. 1988. Sequences homologous to Zfy, a candidate human sex-determining gene, are autosomal in marsupials. Nature 336:780-783.
SCHNIDER-GADICKE, A., P. BEER-ROMERO, L. G. BROWN, G. MARDON, S.-W. LUOH, AND D.C. PAGE. 1989. Putative transcription activator with alternative isoforms encoded by human ZFX gene. Nature 342:708-711.
TEER, J. G. 1984. Ecology and management. Pp. 261-290 in L. K. Halls, ed. White-tailed deer. Stackpole Books, Harrisburg, PA.
TEGELSTROM, H. 1987. Transfer of mitochondrial DNA from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (C. glareolus). J. Mol. Evol. 24:218-227.
TEGELSTROM, H., P.-I. WYONI, H. GELTER, AND M. JAAROLA. 1988. Concordant divergence in proteins and mitochondrial DNA between to two vole species in the genus Clethrionomys. Biochem. Genet. 26:223-237.
TUCKER, P. K., R. D. SAGE, J. WARNER, A. C. WILSON, AND E. M. EICHER. 1992. Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution 46:1146-1163.
WlGGERS, E. P., AND S. L. BEASOM. 1986. Characterization of syrupatric or adjacent habitats of two deer species in west Texas. J. Wildl. Manage. 50:129-134.
WILSON, A. C., R. L. CANN, S. M. CARR, M. GEORGE, U. B. GYLLENSTEN, K. M. HELM-BYCHOWSKI, R. G. HICUCHI, S. R. PALUMBE, E. M. PRAGER, R. D. SAGE, AND M. STONEKING. 1985. Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26:275-400.
WINTER, R. M., E. G. D. TUDDENHAM, E. GOLDMAN, AND K. B. MATTHEWS. 1983. A maximum likelihood estimate of the sex ratio of mutation rates in haemophilia. Hum. Genet. 64:156-162.
WlSHART, J. D. 1980. Hybrids of white-tailed deer and mule deer in Alberta. J. Mammal. 61:714-716.
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|Author:||Cathey, James C.; Bickham, John W.; Patton, John C.|
|Date:||Aug 1, 1998|
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