Abstract
EVOLUTION & SYSTEMATIC BIOLOGY Animal Cells and Systems, 2013 Vol. 17, No. 4, 269–276, http://dx.doi.org/10.1080/19768354.2013.826280 Allelic characterization of the second DRB locus of major histocompatibility complex class II in Ussuri sika deer (Cervus nippon hortulorum): highlighting the trans-species evolution of DRB alleles within Cervidae a,b a,b a Bo Li *, Yanchun Xu and Jianzhang Ma College of Wildlife Resources, Northeast Forestry University, No. 26, Hexing Road, Xiangfang District, Harbin 150040, China; State Forestry Administration Detecting Center of Wildlife, Harbin 150040, China (Received 15 April 2013; received in revised form 12 July 2013; accepted 14 July 2013) MHC (major histocompatibility complex)-DRB variability reflects evolutionarily relevant and adaptive processes within and between populations, and is suitable for the investigation of a wide range of questions in evolutionary ecology. Using motif-specific polymerase chain reaction (PCR), single-stranded conformation polymorphism (SSCP) analyses and direct sequencing, 15 DRB-2 alleles were identified from 43 Ussuri sika deer. Extensive sequence variation was detected at peptide-binding region (PBR) or positively selected sites (PSS) sites among DRB loci, which were proved to be maintained by positive selection. DRB-2 loci of the Ussuri sika deer were strikingly similar to those of red deer after comparing sequences. In phylogenetic analysis, DRB-2 alleles of Ussuri sika deer were not monophyletic with respect to red deer, white-tailed deer, fallow deer, and roe deer sequences. Two DRB-2 alleles of the species tended to cluster together with those of white-tailed deer or red deer with high bootstrap values, respectively. Considering that sika and red deer are closely related, and their hybridization is occasionally seen in areas of range overlap, and their mtDNAs are paraphyletic to white-tailed deer, fallow deer, and other Cervus species, we suggested that these similarities result from trans-species evolution rather than convergent evolution. Keywords: the major histocompatibility complex (MHC); DRB-2; Ussuri sika deer; trans-species evolution; Cervidae Introduction Otting et al. 2002; Doxiadis et al. 2006; Huchard et al. 2006; Suárez et al. 2006). Two mechanisms have been The major histocompatibility complex (MHC) is a posited to explain this phenomenon. First, these allelic multigene family of the vertebrate immune system similarities were explained by the theories of “trans- comprising highly polymorphic loci (Klein 1987). species polymorphism” or “trans-species evolution”: MHC class II (MHC-II) genes are expressed on allelic lineages of common ancestors persist through antigen-presenting cells of the immune system and speciation and are passed from species to species (Klein present processed exogenous antigens to CD4+T helper 1987). Several vertebrate species display trans-species cells (Flajnik & Kasahara 2001; Kelley et al. 2005). The polymorphism, including fish (Ottová et al. 2005), primary role of MHC-II is to recognize various foreign rodents (Seddon & Baverstock 2000; Musolf et al. proteins, a process associated with high sequence varia- 2004), carnivores (Hedrick et al. 2000a; Seddon & tion among alleles of multiple loci, particularly in the Ellegren 2002), ungulates (Hedrick et al. 2000b), and peptide-binding region (PBR) (Ohta 1998). Variation primates (Otting et al. 2002; Huchard et al. 2006). within the PBR suggests that there has been evolutionary The second mechanism is convergent evolution pressure for organisms to combat a wide range of resulting from common adaptive solutions to similar immunological challenges (Abbott et al. 2006). MHC environmental pressures, such as in response to com- variability reflects evolutionarily relevant and adaptive mon pathogens (Kriener et al. 2000). Convergent processes within and between populations, and is evolution results in the emergence of biological struc- suitable for the investigation of a wide range of open tures or species that exhibit similar function and questions in evolutionary ecology. appearance, which evolved through widely divergent Certain MHC loci exhibit extensive genetic poly- morphisms in most vertebrate species (Babik et al. 2005; evolutionary pathways (Gustafsson & Andersson Sachdev et al. 2005). Despite the extensive polymorph- 1994). Convergence at the phenotypic level is a well- recognized and well-established phenomenon, espe- ism within species, a remarkable sharing of polymorphic sequence stretches or motifs, and even identical alle‐ cially at the morphological level. However, evidence les, have been observed among mammalian species for molecular convergence is often either lacking or (Gustafsson & Andersson 1994; Kriener et al. 2000; controversial (Doolittle 1994). *Corresponding author. Email: libo_770206@126.com # 2013 Korean Society for Integrative Biology 270 B. Li et al. Cervidae are ruminants for which many researchers Foster City, CA, USA) under reaction conditions: have reported DRB-2 allelic polymorphism. Mikko 94 °C for 3 min, followed by 35 cycles of 94 °C for et al. (1999) reported no sharing of similar DRB-2 30 sec, 59 °C for 45 sec, 72 °C for 1 min, and a final alleles among 165 ruminants, including five bovids and extension of 5 min at 72 °C. The allelic diversity of five cervids. Only one out of 10 alleles was shared DRB-2 was characterized using SSCP analysis, with between European and North American moose, which 10% non-denaturing polyacrylamide gel (acrylamide: were earlier considered to be subspecies (Mikko & bis-acrylamide=39:1, including 5% glycerin) and using Andersson 1995) but are currently considered separate gel silver staining. To ensure the correctness of mole- species (Wilson & Reeder 2005). Whether a similar cular conformation, all PCR products were analyzed relationship exists between sika deer and other deer twice using the above methods. species has not been well answered. Whether trans- Amplicons were recovered by the second amplifica- species or convergent evolution occurred within Cervi- tion with the same primers. PCR products were purified TM dae also required resolution. In the present study, we using an AxyPrep DNA Gel Extraction Kit (Axy- describe DRB-2 allelic polymorphism in Ussuri sika Gen Biosciences, Hangzhou, China) according to the deer (Cervus nippon hortulorum) using motif-specific manufacture’s instructions. Recovered PCR products polymerase chain reaction (PCR), single-stranded con- were sequenced directly using the primers (LA31s, 5′- formation polymorphism (SSCP) analyses, and direct TCT CTC TGC AGC ACA TTT CCT G-3′ and sequencing. We then compared our data with previous LA32s, 5′-CTT GAA TTC GCG CTC ACC T-3′)on reports for other deer species. This comparison revealed an ABI 3730 DNA Analyzer (performed by BGI, striking interspecific similarity that supported trans- Beijing, China). Consensus sequences were generated species evolution within Cervidae. using SeqMan software (DNAStar Inc., Madison, WI, USA). Material and methods Sequence characterizations and phylogenetic analysis Sampling and DNA isolation Nucleotide sequences of DRB-2 alleles were aligned Muscle and blood samples of 43 Ussuri sika deer were using the ClustalW algorithm of the program MEGA collected from the Songhuahu farm in Jilin province 5.05 (Tamura et al. 2011). Previous analyses showed of China. Only clean-bred Ussuri sika deer named that relatively high proportions of obtained sequences Shuangyang are bred at the farm. These deer were could be artifacts of PCR amplifications (Bryja et al. selected and breed from wild C. nippon hortulorum over 2005). We considered a new sequence variant as a new about 23 years. Tissue samples were stored at 20 °C allele only when it met the criteria proposed by before DNA extraction and genetic analyses. Genomic Kennedy et al. (2002): The allele must be identified DNA was extracted using standard phenol/chloroform either in two separate PCRs from the same individual extraction. or from PCRs from at least two different individuals. Nomenclature of Ussuri sika deer (Ceni DRB) se- quences followed Swarbrick et al. (1995). We also Motif-specific PCR, SSCP analyses, and direct compared our detected allelic sequences with those sequencing reported by Swarbrick et al. (1995) using the ClustalW The DRB-2 locus was amplified by PCR using motif- algorithm. specific primers (LA31G/LA32 and LA31C/LA32), For phylogenetic analysis of deer DRB-2 alleles, we which were modified based on primers LA31 and included published DNA sequences of 3 alleles from roe LA32 (Sigurdardottir et al. 1991). The forward primer deer (Caca DRB, Mikko et al. 1997), 2 alleles from added two bases (GG and GC, respectively) at the fallow deer (Dada DRB, Mikko 1997, unpubl. data), 3′ end of primer LA31 to increase specific amplifica- 9 alleles from reindeer (Rata DRB, Mikko 1997, tions. The redesigned primer accorded to the ninth unpubl. data), 10 alleles from moose (Alal DRB, Mikko motif (GAG or CTG) of DRB-2 locus in sika deer, & Andersson 1995), 18 alleles from red deer (Ceel DRB, which differed from other Cervidae (Brown et al. 1993). Fernández-de-Mera et al. 2009), and 18 alleles from A 50 µL PCR reaction mix contained about 100 ng white-tailed deer (Odvi DRB, Van Den Bussche et al. DNA template, 1×PCR buffer (10 mM Tris–HCl, 1999). But some allelic sequences of red deer in pH 8.3; 50 mM KCl; and 1.5 mM MgCl ), 0.2 mM Genbank (reported by Swarbrick et al. 1995) were dNTP, 0.2 µM of each primer, and 2.5 units TaqTM excluded from our phylogenetic analyses because they DNA polymerase (TaKaRa Biotechnology Dalian were shorter sequences. In addition, partial homologous Co., China). Amplifications were carried out on a sequences of sika deer were also excluded, because we could not determine whether they were artifacts GeneAmp PCR System 9700 (Applied Biosystems, Animal Cells and Systems 271 Figure 1. Conjectural amino acid sequences of DRB-2 alleles in Ussuri sika deer. Dots indicate identical amino acids with reference to Ceni_DRB3. The NGT glycosylation site is shaded, and cysteine residues (C) are underlined. 272 B. Li et al. with small nucleotide differences from our detected deML, which is contained in the PAML 3.14 program allelic sequences. suite (Yang 1997). The presence of PSS, characterized A neighbor-joining (NJ) method was used as im- by ω=d /d >1, was investigated for the DRB-2 amino N S plemented in MEGA 5.05. The T92+G model (Tamura acid sequences in Ussuri sika deer. We compared the 3-parameter, Gamma distributed, G=0.3224) was se- null model (without positive selection), where ω<1 lected as the best-fitting model of DNA substitution by (model M7), with a model allowing an additional class the Bayesian information criterion (BIC) in the same of sites where ω>1 to account for the possible program. To reconstruct the tree topology, maximum occurrence of PSS (model M8) using a likelihood ratio likelihood (ML) analysis was performed using Phyml test (LRT; Yang & Bielawski 2000). In cases where M8 3.0 (Guindon et al. 2010) with the GTR+I+G model fit the data-set better than M7, PSS were subsequently (I=0.1459, G=0.4245), which was the best-fit model identified using Bayes empirical Bayes (BEB) analysis selected by the Akaike information criterion (AIC) in (Yang et al. 2005). M7 and M8 have proven to be more Modeltest 3.7 (Posada & Crandall 1998). The confidence robust toward intragenic recombination than other limits of branches in NJ and ML trees were assessed using models, as has Bayes’ prediction of sites under positive non-parametric bootstrapping searches of 1000 replicates selection (Anisimova et al. 2003). (Felsenstein & Kishino 1993). Two bovid DQB sequences (Bota-DQB, DQ089658 and DQ089659) were used as outgroups. Topologies of trees with bootstrap values 70% Results or greater were regarded as sufficiently resolved (Huel- Sequences characterizations and phylogenetic analysis senbeck & Hillis 1993), and those between 50% and 70% Nucleotide sequence analysis of 249 bp from the as weakly supported. DRB-2 region of 43 Ussuri sika deer revealed 15 distinct alleles (accession numbers: DQ225342, DQ225347, Testing for selection DQ225349, DQ225352, DQ225353, DQ225359, and FJ864326–FJ864334). Most deer yielded more than We used the program MEGA 5.05 for molecular two sequences. Each sequence had a distinct predicted evolutionary analyses to calculate relative frequencies sequence of 83 amino acids (Figure 1). None of the of synonymous (d ) and nonsynonymous (d ) substitu- S N above sequences involved insertions, deletions, or stop tions by the method of Nei and Gojobori (1986) with codons. The sequences showed two cysteine residues at the Jukes and Cantor (1969) correction for multiple positions 7 and 71, respectively. NGT glycosylation sites substitutions. Separate tests were conducted for sites were also present in fourteen sequences with one predicted to be involved in antigen recognition, assum- exception of Ceni DRB26 (one mutation N→K). ing concordance with human PBR (Brown et al. 1993), Considering all above sequences, we documented a as well as for non-PBR sites, and then for positively selected sites (PSS) and non-PSS. A global test was also total of 87 variable nucleotide positions (34.9%) and conducted using all sequences to calculate the overall corresponding 42 (49.4%) amino acids variations. The values of d and d , and the rates ω were tested for divergence across the nucleotide and the inferred amino N S significant differences with a Z-test. acid sequences between pairs of alleles ranged from More rigorous analyses of selection were performed 4.0% (Ceni DRB8 vs. Ceni DRB25) to 17.3% (Ceni using likelihood ratio modeling in the program Co- DRB3 vs. Ceni DRB14). Among 16 PBRs defined by Figure 2. Amino acid variability is plotted among15 DRB-2 allelic sequences in Ussuri sika deer. Letter “h” indicated PBRs defined by homology with HLA. Significant PSS are indicated by black triangles. Animal Cells and Systems 273 homology with human leukocyte antigen (HLA) (Brown et al. 1993), 15 were variable and 1 was conserved (position 74, Figure 2). Twenty-three of 67 non-PBR sites (34.3%) were polymorphic and most were located next to a PBR. After comparison with detailed allelic sequences of other deer species, we found high proportions of shared identical sequences among alleles from Ussuri sika deer and palaearctic or nearctic red deer reported by Swarbrick et al. (1995). These included Ceni DRB13 and Ceel DRB45 at 90.36% and Ceni DRB8 and Ceel DRB35 at 89.95%. In other words, there were identical sequence motifs at DRB-2 loci between sika and red deer, possibly a response to common pathogens. NJ phylogenetic analyses yielded tree topologies similar to the ML tree, but phylogenetic relationships had less or more statistical support (Figure 3). The trees revealed monophyletic relationships for moose and reindeer alleles. Ceni DRB alleles found in this study were not monophyletic with respect to red deer, white- tailed deer, fallow deer, and roe deer sequences. More- over, Ceni DRB23 tended to cluster with those of white-tailed deer (Odvi DRB11) with high bootstrap values (NJ and ML bootstrap values were 91% and 89%, respectively) rather than alleles from sika deer. A similar relationship was seen between Ceni DRB3 and Ceel DRB7 (NJ and ML bootstrap values were 78% and 84%, respectively). Testing for selection The species-specific codon sites affected by positive selection (PSS) were analyzed by ML analysis (Figure 2). The LRT statistic for comparing M7 (β) and M8 (β and ω)is2Δ ln L=2×((1306.517) (1331.340))=49.64 (ln L=log-likelihood value). The comparison with a χ distribution indicated that our data fitted the M8 model significantly better than the M7 model (d.f.=2, P<0.001). M7 was thus rejected in favor of M8. We detected 20 PSS sites, among which 13 were statistically significant (P<0.05) according to BEB analysis, including positions 3, 5, 17, 18, 26, 36, 49, 52, 53, 59, 62, 63, and 78 (the nonsignificant PSS were excluded in subsequent analyses, Figure 2). Eight significant PSS superposed with the PBR defined by Figure 3. Phylogenetic tree reconstructed from nucleotide homology with HLA (Figure 2). The remaining PSS sequences of DRB-2 alleles within Cervidae. Numbers at (positions 17, 18, 26, 36, and 52, Figure 2) were situated branch-points represent bootstrap support values and only within a distance of one to five amino acids of the PBR. bootstrap values ≥50% are shown. ML and NJ bootstrap Eight human PBRs (positions 1, 20, 22, 29, 30, 66, 70, values are the former and the latter of diagonal, respectively. Common name of each species corresponding to each DRB-2 and 74, Figure 2) were also excluded from Ussuri sika allele is indicated at the right side of the tree. Two bovid DQB deer PSS. sequences (Bota-DQB) are used as outgroups. Frequencies of synonymous and nonsynonymous substitution were calculated separately for PBR and synonymous substitutions among PBR sites (d = non-PBR sites (Table 1). Nonsynonymous substitutions occurred at a significantly greater frequency than 0.609±0.115, d =0.163±0.075, P <0.001). But these S 274 B. Li et al. Table 1. Estimates of d and d (±SD) analyzed over all N S cult to identify two particular loci from these sequences codon positions, partitioned into PBR and non-PBR, PSS, as we did not perform cDNA analysis. and non-PSS, respectively. The high levels of allelic diversity found within the studied Ussuri sika deer population were similar Positions nd d ω p N S to those found in red deer (Swarbrick et al. 1995; PBR 16 0.609±0.115 0.163±0.075 3.73 <0.001 Fernández-de-Mera et al. 2009), white-tailed deer (Van Non-PBR 67 0.066±0.015 0.069±0.021 0.95 ns Den Bussche et al. 1999), and Père David’s deer (Wan PSS 13 0.826±0.096 0.223±0.114 3.70 <0.001 et al. 2011). In contrast, the DRB-2 genetic diversity Non-PSS 70 0.068±0.015 0.064±0.018 1.06 ns reported in moose and reindeer is greatly reduced All 83 0.141±0.025 0.085±0.021 1.66 ns (Mikko & Andersson, 1995; Mikko et al. 1999; Wilson et al. 2003), possibly due to limited parasite exposure n, number of codons in each category; ns, nonsignificant. in boreal ecosystems and/or bottlenecks (Mikko & Andersson, 1995; Ellegren et al. 1996; Mainguy et al. two frequencies were nearly equal in non-PBR sites. A 2007). similar pattern was also exhibited in PSS and non-PSS The number and distribution of polymorphisms (Table 1). This suggested that high variation at PBR or within the Ussuri sika deer DRB-2 amino acid sequence PSS sites was maintained by positive selection. was similar to levels detected in white-tailed deer, red deer, and Père David’s deer alleles (Swarbrick et al. 1995; Van Den Bussche et al. 1999; Fernández- Discussion de-Mera et al. 2009; Wan et al. 2011). Nonsynonymous Several previous studies reported that relatively high substitutions occurred more frequently than synon- proportions of obtained sequences could be artifacts of ymous substitutions, which were congruously presented PCR amplifications or cloning (Kennedy et al. 2002; at PBR or PSS sites. This result denoted a strong Longeri et al. 2002; Bryja et al. 2005). Herein, we used positive selection pressure on certain amino acids motif-specific PCR, SSCP analysis, and direct sequen- within the DRB-2 sequence of Ussuri sika deer, which cing to detect DRB-2 alleles in Ussuri sika deer for the was consistent with reports in other deer species and first time. Our modified methods had two obvious primarily maintained by pathogen-driven selection advantages. First, using motif-specific PCR had poten- (Van Den Bussche et al. 1999; Lohm et al. 2002; tial to increase the specific of amplifications and Wegner et al. 2003; Harf & Sommer 2005; Schad et al. decrease mismatch among multi-sequences. Second, 2005). However, we could not exclude a false positive direct sequencing of amplicons curtailed the process selection for these sites in the absence of accurate descriptions of protein structures of DR molecules in of cloning and feeble signal point mutations could be the target species. Wong et al. (2004), however, used leached in the sequencing. Our modified methods simulations on HLA data to demonstrate that the ML reduced the risk of producing artificial sequences as method has power and accuracy in detecting positive compared with the previous approaches to PCR– selection over a wide range of parameter values. SSCP–cloning sequencing. This was also one major High similarities of DRB-2 alleles were found reason that we excluded from our data analyses some between Ussuri sika deer and palaearctic or nearctic sika deer DRB-2 alleles obtained from Genbank. red deer. These alleles could not be artifacts of PCR Combined with the above criteria for new alleles, the amplifications, as they were also observed by other method provided a new approach for investigating researchers (AY679496, Wu et al. 2004, unpubl. data). DRB-2 polymorphism of deer species. Using phylogenetic analysis, Ceni DRB alleles were not DRB loci are often duplicated independently in monophyletic with respect to four deer species. More- several vertebrates, including functional loci and pseu- over, two Ceni DRB alleles always clustered with those dogenes (Hughes & Nei 1990; Yuhki et al. 2003; Wan of white-tailed deer and red deer. Considering that sika et al. 2011). We detected 15 distinct alleles of DRB-2 in and red deer are closely related, and they occasionally Ussuri sika deer. These sequences would possibly be hybridize when populations are sympatric (Senn & functional because they showed some characteristics Pemberton 2009), but based on cytochrome b gene, of forming one DR molecule, such as cysteine residues ATPase and D-Loop sequences their mtDNAs are (Schaschl et al. 2004) and N-linked glycans (Nag et al. paraphyletic to white-tailed deer, fallow deer, and other 1992). Numerous deer producing more than two se- Cervus species (Polziehn & Strobeck 1998; Tamate et al. quences suggested that DRB-2 was duplicated in Ussuri 1998; Cook et al. 1999; Li et al. 2003), we suggest that sika deer. This was similar to red deer (Swarbrick the above characters resulted from trans-species evolu- et al. 1995; Fernández-de-Mera et al. 2009) and Père tion rather than convergent evolution. The latter is due David’sdeer(Wan etal. 2011). It was, however, diffi‐ to common adaptive solutions to similar environmental Animal Cells and Systems 275 Fernández-de-Mera IG, Vicente J, Pérez de la Lastra JM, pressures and is unlikely in non-sympatric deer species. Mangold AJ, Naranjo V, Fierro Y, De La Fuente J, The same evolutionary pattern has been observed in Gortázar C. 2009. Reduced major histocompatibility many other vertebrates (Hedrick et al. 2000a, 2000b; complex class II polymorphism in a hunter-managed Seddon & Baverstock 2000; Otting et al. 2002; Seddon isolated Iberian red deer population. J Zool. 277:157–170. Flajnik MF, Kasahara M. 2001. 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Journal
Animal Cells and Systems
– Taylor & Francis
Published: Aug 1, 2013
Keywords: the major histocompatibility complex (MHC); DRB-2; Ussuri sika deer; trans-species evolution; Cervidae
