Supporting Information http://www.genetics.org/cgi/content/full/genetics.110.116228/dc1 Sex-Linked Inheritance in Macaque Monkeys: Implications for Effective Population Size and Dispersal to Sulawesi Ben J. Evans, Laura Pin, Don J. Melnick and Stephen I. Wright Copyright 2010 by the Genetics Society of America DOI: 10.1534/genetics.110.116228
2 SI B. J. Evans et al. FILE S1 Additional information on sampling locations, PCR primers, and MIMAR commands used in this study Supplementary data on genetic samples used in this study. Sample ID Species Sex Locality Information Other WM0011 M. maura male Bontobahari, Sulawesi Selatan Wild caught WM009 M. maura male Bontobahari, Sulawesi Selatan Wild caught PM1014 M. hecki male 60km west of Gouonlalo, Paguyaman town; Sulawesi Island Friend caught it PM545 M. tonkeana (East) male Malik; Pangimanan district; Owner caught it Sulawesi Island PF559 M. tonkeana (West) Female Salukondo Forest; Sulawesi Tengah PF560 M. tonkeana (West) Female Dmu Forest; Sulawesi Tengah Owner caught it PM561 M. tonkeana (West) male Tambaro near Tagolu Lagi disrict; Sulawesi Island Owner's dog helped chatch it in the forest PM574 M. ochreata male Wosu Forest; Sulawesi Tengah Owner caught it PM582 M. tonkeana (West) male Lee forest west of Gontara; Owner caught it as baby Sulawesi Island PF599 M. tonkeana (West) female Betwee Donggala and Towale; Brother of owner caught it Sulawesi Tengah PM604 M. tonkeana (West) male Enrekang; Sulawesi Island Caught on mountain 2km away by father of owner PM638 M. hecki male 1/2km north Marantale; Sulawesi Island PM704 M. ochreata male 15km north of Kolaka; Sulawesi Island PM655 M. nigrescens male 5 km east of Bilungala; Sulawesi Island PM661 M. nigra male Kauditan; Klabat Mountain, 6km from Kauditan; Sulawesi Island PM665 M. nemestrina nemestrina male Kariabarun 7km from Karanbaurun in between Puruajaya and Sungai Merdeka; 75km from Balikpapan 45km from Saurarande; Eastern Borneo Island PM3003 M. nemestrina nemestrina male Pontanak Camp Silva; Western Borneo Island; origin unknown PM1210 M. nemestrina nemestrina male Probably from Tongarong; Borneo Island; origin unknown PM1211 M. nemestrina nemestrina male Sampled near Balikpapan in a small zoo; Borneo Island; origin unknown PM3005 M. nemestrina nemestrina male Pontianak Zoo PM3005 M. nemestrina nemestrina male Pontianak Zoo; Western Borneo Island Caught by trap Caught by owner in trap for monkeys Caught with hands while young, had no hair, still very young; 1 year Owner caught with rope trap; 4 months here; excelennt locality; same owner as PF660 Owner caught it when fell out of tree Given by a man from Sangao near boarder with Malaysia PF1214 M. nemestrina nemestrina female Police Station in Samarinda PM1215 M. nemestrina nemestrina male Near Sauramider; Borneo Island Caught by owner 7 years; near Sauramider; good locality info PM664 M. nemestrina nemestrina male Samboja; Barabai; South Bought Kalimantan; Borneo Island PM1206 M. nemestrina nemestrina male Between Binnang and Martapura; Borneo Island Caught by neighbours when young Suka M. nemestrina nemestrina male PF1204 M. nemestrina nemestrina female Near Buntok; Borneo Island Caught by owner PF1207 M. nemestrina nemestrina female Near Kandangan; Borneo Island Caught by owner PF1208 M. nemestrina nemestrina female Paringin; Borneo Island; origin unknown pag930 M. nemestrina pagensis male Ngsang M. nemestrina nemestrina female Ngsang, Sumatra Island PM666 M. fascicularis male Near Bargut river; Borneo Island Caught with hands
B. J. Evans et al. 3 SI Supporting material on PCR primers used in this study Mitochrondrial DNA CYT-L (ROOS et al. 2003) 5 AAT GAT ATG AAA AAC CAT CGT TTT A 3 CYT-H (ROOS et al. 2003) 5 AAA ATC CCC TTC CAC CCC TAC TA 3 CTYB_14658_FOR2 5 CTC CCR TGR GGC CAA ATA TCA TTC TG 3 CYTB_15403_REV1 5 CAR GTT CAY TTG AGT AGG TTG TTT TC 3 CTYB_15277_FOR4 5 GAA GCG AAC CAG TAR TCC AAC C 3 DLOOP_16073_REV3 5 TAA GRG GAA CGT GTG GGC G 3 Y chromosome DNA AMLEYforward3 5 CAG AGC ATG ATA AGA CCA CCA 3 AMLEYreverse 5 AGA CCC TGA GTT GTT GGA CC 3 DBYforward2 DBYreverse2 DBY_internal_forward1 DBY_internal_reverse1 5 CAC TGT GAG TAA ACA AAG CC 3 (PCR) 5 CAC CCT CTC TAA TAA TCA T 3 (PCR) 5 GTC TCG TTC TGT CAC TCA G 3 (Sequencing) 5 GTT TCC TAC ACG TCC TGT ACG 3 (Sequencing) PRKYforward 5 GTG CTG ACA CCT AGC TGA CGG T 3 PRKYreverse5 5 ACA CTC CTC TRT ATG CCC 3 SMCYforward 5 GTG TCT GAG CCC TGT TAC AG 3 SMCYreverse 5 ACA AGA CTG GAG CTA CAA G 3 SMCYreverse2 5 GAA TGG AGC AAA GGG ACT AGG C 3 SW2 (TOSI et al. 2000) 5 CTT GAG AAT GAA TAC ATT GTC AGG G 3 SW3B (TOSI et al. 2000) 5 AGG TGT TTG TAG CCA ATG TTA CCC G 3 TBL1Yforward 5 AGT GCC CTT TAA ATG CCT TC 3 TBL1Yreverse2 5 CCT ATG TCT GCA CAC ATT CCA TCA 3 USP9Yforward 5 CTG TTC TAG TTA CAA GAG AAC ATT TG 3 USP9Yreverse 5 ATC CTA GAA GCC AAA TAA AAA C 3 UTYforward2 5 AGA GTT TTC TGT ATA TGC 3 UTYreverse2 5 CCA CAC TAA CCT GCA TGC T 3 ZFYforward 5 ATT CAT GAG GAG ACC AGA AGT TTG ATT A 3 ZFYreverse 5 ATG TCT ACA TTG GTG CAT TTT TTT ACC T 3 X chromosome DNA AMLEXforward 5 ATC AGT GAG TTT CTA TAT T 3 AMLEXreverse 5 AGA TCC TTG GTT GTC GGA GA 3 CXorf15for2 5 TGG CAA GAA GCA AGC TAG AGT CTC 3 CXorf15rev1 5 CTT TCC TTC TTC CCC TGT TGA TAC 3
4 SI B. J. Evans et al. DBXforward 5 AGA CAA AAA AGG GAG CAG ATT CT 3 DBXreverse 5 CAG CTG CTG CTT GTA TGA CTA CTA CT 3 EF1AX_for5 5 AGT ATG CTC AGG TAA TCA AAA TGT TG 3 EFiAX_rev5 5 GGG CTG ACT GCT TGA GCT CAG G 3 NLGN4Xforward 5 GAC ATG GTA GAA TGC CTG CG 3 NLGN4Xreverse 5 CGT GTG CTC GTG CAA GTG GCA 3 PRKXforward 5 TCT GTC TGT ACA CAC ATT TTG G 3 PRKXreverse 5 CTT CCT GCC CAC CGG CTC TTG G 3 RBMXfor1 5 GTT GCG CAG TAG TGC TAG CGG C 3 RBMXrev2 5 TAA AAA CCG CGT GTA AAA GAC 3 SOX3forward3 5 CAG CCA GAC TGT GAA TGC GAC C 3 SOX3reverse3 5 GAC GTT CAT GTA GCT CTG AGC 3 TBL1Xforward 5 AGM GCC CTT TAA GTG TGT TT 3 TBL1Xreverse 5 GCC TCC TAT GTC TGC ATG RGC 3 TMSB4Xforward 5 GCT CTT CCT CAC GCT CGC TC 3 TMSB4Xreverse 5 TAC AGT GCA TAT TGG CGG CG 3 USP9Xforward 5 GGA TTT TAA TAG AAC ATC TRG TAA C 3 USP9Xreverse 5 TAC TAA GAA GCT AAA CTC TC 3 UTXforward 5 CTG TAC ATT CTC ART TTG CT 3 UTXreverse 5 ATT TCA GCA TTC TGA TCA T 3 ZFXforward 5 AGA AAC TGG AAC AGA ACT TGG TTT G 3 ZFXreverse 5 ATG TCT ACA CTG GTG CAT TTT TTT GCC C 3 Autosomal DNA macaque_newbeta_for4 5 GGT ATG GCT GTC ATC ACT TAG 3 macaque_newbeta_rev4 5 GGG GAA AGA AAA CAT CAA GGG TC 3 CCL2_Forward (WRIGHT et al. 2006) 5 CCG AGA TGT TCC CAG CAC AG 3 CCL2_Reverse (WRIGHT et al. 2006) 5 CTG CTT TGC TTG TGC CTC TT 3 NRAMP_intron5_for (DEINARD and GLEN SMITH 2001) TCA TCG G 3 NRAMP_intron5_rev (DEINARD and GLEN SMITH 2001) AGA AGA AGG 3 5 ACA TGC AGG AAG 5 CGA GGA AGA GGA
B. J. Evans et al. 5 SI AFP_M13tag_for (STEVISON and KOHN 2009) 5 GTA AAA CGA CGG CCA GTC ACC ACT GCC AAT AAC AAA ATA AC 3 AFP_M13tag_rev (STEVISON and KOHN 2009) 5 AAC AGC TAT GAC CAT GCT GCA GTA CAT TGG TAA GAA TCC A 3 APOE_M13tag_for (STEVISON and KOHN 2009) 5 GTA AAA CGA CGG CCA GTG GTC GCT TTT GGG ATT ACC T 3 APOE_M13tag_rev (STEVISON and KOHN 2009) 5 AAC AGC TAT GAC CAT GCT TCA ACT CCT TCA TGG TCT CAT C 3 B2M_M13tag_for (STEVISON and KOHN 2009) 5 GTA AAA CGA CGG CCA GTC CAA AGA TTC AGG TTT ACT CAC G 3 B2M_M13tag_rev (STEVISON and KOHN 2009) 5 AAC AGC TAT GAC CAT GCC ATG ATG CTG CTT ACA TGT CT 3 TTR_M13_for (STEVISON and KOHN 2009) 5 GTA AAA CGA CGG CCA GTC CTC GCT GGA CTG GTA TTT G 3 TTR_M13tag_rev (STEVISON and KOHN 2009) 5 AAC AGC TAT GAC CAT GGA CCA TCA GAG GAC ACT TGG ATT 3 Sequencing primers for AFP, APOE, B2M, and TTR: M13_minus20_for 5 GTAAAACGACGGCCAGT 3 M13_minus24_rev 5 AACAGCTATGACCATG 3 IRBP_forward 5 AAA TGT GGC TCT CCC AAG TG 3 IRBP_reverse 5 CCT GGA GCA CCT GTC TTC TC 3 ASIP_for1 5 CCT CTT ACC ATT ACC CCG A 3 ASIP_Ag2R4_Reverse (MUNDY and KELLY 2006) 3 CTG TTG ACA GGA GTT CTG TGA TTC 3 ATXN10_L2_modified 5 AGT AAT TGC TCA AAG ATT AAA C 3 ATXN10_R1_modified 3 TTC AGA GAC TTC AGT AAA GAC AGG 3 GPR15forward 5 TGT GTT CCT GAC TGG AGT GC 3 GPR15reverse 5 CAG CCA GGA GAC AAG AAA GG 3 KFL10_for 5 CCT TCC TCA GAG ACG GTC AT 3 KFL10_reverse 5 TCA CAG CCA AAA CCT CTT CA 3 PDYN_forward1 5 GAA TGG GAG AGA TGC CAG AG 3 PDYN_reverse1 5 ACC GAG TCA CCA CCT TGA A 3 TRIM22_modified_Forward 5 CTC AAT GCC ATA AGA CAC ACC TAT CCC 3 TRIM22_335_reverse (SAWYER et al. 2007) 5 GAA GTG GGT AAG GGA ATT AGA ACA C 3
6 SI B. J. Evans et al. TRIM22_340_sequencing_forward (SAWYER et al. 2007) 5 GGA AAG ATT GCC TGG ATC CTG G 3 TRIM22_375_sequencing_reverse (SAWYER et al. 2007) 5 GAG GTC TGT ATT TGG AAT AAA CAT TTG C 3 Supporting material on demographic analysis: The relative N e of adna, xdna, ydna, and mtdna was calculated in a Wright-Fisher idealized population with either varying degrees of adult sex ratio skew or varying levels of female migration. Given the data and these expectations, the likelihood of alternative values of sex ratio skew or female migration was then evaluated using mlhka (WRIGHT and CHARLESWORTH 2004). For the model with a skewed sex ratio, assuming panmixia, effective population sizes of mtdna and ydna are respectively equal to half the effective number of females (N ef ) and males (N em ) in the population (HEDRICK 2007). N e is equal to (N k -1) / (k+v k /k-1), where k and V k are the mean and variance of progeny numbers (LANDE and BARROWCLOUGH 1987). When the number of female offspring per female is Poisson distributed with a mean of one (i.e. constant population size and sex ratio), k = V k and N e-mtdna = N ef /2 = (N f 1) / 2. When the number of male offspring per male is Poisson distributed with a mean of one, N e-ydna = N em /2 = (N m 1) / 2. N e-xdna is equal to 9N ef N em / (2N ef +4N em ) (WRIGHT 1933) and the effective population size of autosomal DNA (N e-adna ) is 4N em N ef / (N em +N ef ) (WRIGHT 1931). For the model with sex-biased migration, under the standard island model with s subpopulations of effective size (N s ) in which migration occurs from one subpopulation to another with a probability of m / (s-1), N e is equal to sn s (1+(s-1) 2 / (4N s ms 2 )) (NEI and TAKAHATA 1993). If dispersal is sex-biased, N e-xdna of the entire population can be calculated by using xdna values for m and N s. Dispersal of xdna to all subpopulations is equal to (2m f + m m ) / 3 where m m and m f are the dispersal probabilities of males and females to all subpopulations. N e-xdna of each subpopulation (N s-xdna ) is equal to 9N ef N em / (2N ef +4N em ). When the number of female progeny per female is Poisson distributed with a mean of 1, N ef is equal to s(n sf )[1+(s-1) 2 / (4N sf m f s 2 )] (NEI and TAKAHATA 1993), where N sf is the effective number of females per subpopulation (i.e., the number of females per subpopulation minus 1). N em can be calculated using the
B. J. Evans et al. 7 SI values of N e and m corresponding to males, and N e-mtdna and N e-ydna are respectively equal to half of these values. For the model with sex-biased dispersal, a population of 10,000 individuals with an equal proportion of each sex, a probability of male migration equal to 0.1 individuals per generation, and 10 equally sized subpopulations were assumed. These parameter values cause the ratio of N e-ydna to N e-xdna to be close to the ideal expectation with an equal proportion of males and females, irrespective of the female migration probability because at this or a higher level of male migration, variation in adna and xdna is homogenized by paternal gene flow (See Fig. 1b in main text). Supporting material on commands for MIMAR analysis: Below are the command lines used for each of the 4 models evaluated using MIMAR. Model 1: Samples from M. tonkeana and M. nemestrina, asymmetric ongoing migration with Borneo and intralocus recombination: Command line: mimar 4000 10000 27 -lf mimar_pamlstar_tonk.in -u 4.44e-9 -t u 0.000005 0.008 -n u 0.000007 0.008 -ej u 0 2500000 -N u 0.0000001 0.025 -m 1 2 l -8 3 - m 2 1 l -8 3 -i 1000 -x 10 -y t -L 90 -v 0.0008 0.0008 250000 0.0025.3.3 -r e 1.667 -o exsoutput Model 2: Samples from M. tonkeana and M. nemestrina, with intralocus recombination but no migration with Borneo Command line: mimar 4000 10000 27 -lf mimar_pamlstar_tonk.in -u 4.44e-9 -t u 0.000005 0.009 -n u 0.000007 0.01 -ej u 0 1700000 -N u 0.0000001 0.025 -i 1000 -x 10 - y t -L 90 -v 0.0009 0.001 300000 0.003.3.1 -r e 1.667 -o exsoutput Model 3: Samples from all Sulawesi species and M. nemestrina included, asymmetric ongoing migration with Borneo and intralocus recombination: Command line: mimar 4000 10000 29 -lf mimar_pamlstar.in -u 4.44e-9 -t u 0.000005 0.008 -n u 0.000007 0.006 -ej u 0 2000000 -N u 0.0000001 0.01 -m 1 2 l -8 3 -m 2 1 l -8 3 -i 1000 -x 10 -y t -L 90 -v 0.0008 0.0006 200000 0.0002.7.7 -r e 1.667 -o exsoutput Model 4: Samples from all Sulawesi species and M. nemestrina included, with intralocus recombination but no migration with Borneo: Command line: mimar 4000 10000 29 -lf mimar_pamlstar.in -u 4.44e-9 -t u 0.000005 0.01 -n u 0.000007 0.008 -ej u 0 1700000 -N u 0.0000001 0.05 -i 1000 -x 10 -y t -L 90 -v 0.001 0.0008 170000 0.003.3.1 -r e 1.667 -o exsoutput
8 SI B. J. Evans et al. References DEINARD, A., and D. GLEN SMITH, 2001 Phylogenetic relationships among the macaques: evidence from the nuclear locus NRAMP1. Journal of Human Evolution 41: 45-59. HEDRICK, P. W., 2007 Sex: Differences in mutation, recombination, selection, gene flow, and genetic drift. Evolution 61: 2750-2771. LANDE, R., and G. F. BARROWCLOUGH, 1987 Effective population size, genetic variation, and their use in population management, pp. 87-124 in Viable Populations for Conservation, edited by M. E. SOULÉ. Cambridge University Press, Cambridge. MUNDY, N. I., and J. KELLY, 2006 Investigation of the role of the agouti signaling protein gene (ASIP) in coat color evolution in primates. Mammalian Genome 17: 1205-1213. NEI, M., and N. TAKAHATA, 1993 Effective population size, genetic diversity and coalescence time in subdivided populations. Journal of Molecular Evolution 37: 240-244. ROOS, C., T. ZIEGLER, J. K. HODGES, H. ZISCHLER and C. ABEGG, 2003 Molecular phylogeny of Mentawai macaques: taxonomic and biogeographic implications. Molecular Phylogenetics and Evolution 29: 139-150. SAWYER, S. L., M. EMERMAN and H. S. MALIK, 2007 Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLoS Pathogens 3: e197. STEVISON, L. S., and M. H. KOHN, 2009 Divergence population genetic analysis of hybridization between rhesus and cynomolgus macaques. Molecular Ecology 18: 2457-2475. TOSI, A. J., J. C. MORALES and D. J. MELNICK, 2000 Comparison of Y-chromosome and mtdna phylogenies leads to unique inferences of macaque evolutionary history. Molecular Phylogenetics and Evolution 17: 133-144. WRIGHT, E. K., J. E. CLEMENTS and S. A. BARBER, 2006 Sequence variation in the CCchemokine ligand 2 promoter of pigtailed macaques is not associated with the incidence or severity of neuropathology in a simian immunodeficiency virus model of human immunodeficiency virus central nervous system disease. Journal of Neurovirology 12: 411-421. WRIGHT, S., 1931 Evolution in Mendelian populations. Genetics 16: 97-159. WRIGHT, S., 1933 Inbreeding and homozygosis. Proceedings of the National Academy of Sciences 19: 411-419. WRIGHT, S. I., and B. CHARLESWORTH, 2004 The HKA test revisited: a maximumlikelihood ratio test of the standard neutral model. Genetics 168: 1071-1076.
B. J. Evans et al. 9 SI FIGURE S1. Posterior distributions of parameters of (A) 4Neμ of macaque monkey populations on Borneo ( B ), combined data from all Sulawesi species except M. brunnescens ( S ), and the ancestor of these populations before divergence ( A ) for models with and without migration. (B) divergence time (T) in generations for each model. (C) migration from Borneo to Sulawesi (m BS ) and from Sulawesi to Borneo (m SB ) in the model with asymmetric migration.
10 SI B. J. Evans et al. FIGURE S2. Genealogies of mtdna and ydna. Labels follow Fig. 5.