Evolutionary and dispersal history of Eurasian house mice Mus musculus clarified by more extensive geographic Title sampling of mitochondrial DNA

Suzuki, Hitoshi; Nunome, Mitsuo; Kinoshita, Gohta; Aplin, Ken P.; Vogel, Peter; Kryukov, Alexey P.; Jin, Mei-Lei; Author(s) Han, Sang-Hoon; Maryanto, Ibnu; Tsuchiya, Kimiyuki; Ikeda, Hidetoshi; Shiroishi, Toshihiko; Yonekawa, Hiromichi; Moriwaki, Kazuo

Heredity, 111(5), 375-390 Citation https://doi.org/10.1038/hdy.2013.60

Issue Date 2013-11

Doc URL http://hdl.handle.net/2115/55342

Type article (author version)

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Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP Table 1 Data summary for populations, haplotypes and nucleotide diversity of Mus muculus Marker Subspecies group N H Hd S Pi (%) k Control Region (CR) CAS 86 42 0.958 54 1.195 6.91 MUS 132 66 0.981 58 0.842 5.16 DOM 531 370 0.997 163 1.053 8.3 GEN 6 6 1 16 1.029 6.26 NEP* 2 2 1 12 1.376 12 Nepal** 5 5 1 22 2.703 11

Cytochrome b (Cytb) CAS 38 17 0.895 44 0.468 4.48 MUS 88 49 0.956 67 0.407 4.62 DOM 53 31 0.968 57 0.526 5.07 NEP 2 1 1 12 1.053 12 Abbreviations: N, number of samples; H, number of haplotypes; Hd, haplotype diversity; S, number of polymorphic sites; Pi, nucleotide diversity; k, mean number of pairwise differences among sequences. *NEP: HS1467, HS1523. **Nepal: HS1467, HS1523, AF074524, AF074525, AF074526 Table 2 Divergence time estimation using mitochondrial cytochrome b sequences (1140 bp) Node* TMRCA estimated Divergence time** Confidence interval† A DOM/NEP and CAS/MUS 0.4591 0.3250 - 0.4808 B CAS and MUS 0.4179 0.2863 - 0.5432 C DOM and NEP 0.3719 0.2385 - 0.4805 D CAS 0.2173 0.1340 - 0.2947 E MUS 0.1509 0.0812 - 0.2136 F DOM 0.1333 0.0690 - 0.1478 G NEP 0.1408 0.0623 - 0.1852 *See Figure 7 for detail. **Mean divergence times (million years ago; mya) were obtained from the BEAST analysis. Divergence times were calculated on the assumption of 1.7 mya for the divergence of Mus muculus and Mus spretus. †CI values are 95% highest posterior density interval. Table 3 Estimation of population expansion times (year before present) based on mitochondrial cytochrome b sequences (1140 bp) Subsitution rates (myr/site/lineage) Group Main range N Pi (%) Tajima's D Tau (Confidence interval) SSD 2.5% 10% 20% CAS-1 S and E Asia 34 0.195 -1.93* 1.835 (1.279~2.556) 0.00353 32,200 8,000 4,000 CAS-1a Yunnan, N Japan 17 0.08 -1.237 - CAS-1b India, SE Asia 17 0.202 -2.583* 1.734 (0.436~3.676) 0.01005 30,000 7,600 3,800 MUS-1 N Eurasia 76 0.304 -2.257** 1.725 (1.724~2.352) 0.07956** 30,200 7,500 3,800 MUS-1a E Europe 9 0.244 -0.255 - MUS-1b N 26 0.392 -1.952* 4.920 (2.941~6.468) 0.00451 86,000 21,000 10,800 MUS-1c Korea, Japan 41 0.12 -2.190* 1.527 (0.746~2.535) 0.01595 26,000 6,600 3,300 MUS-2 China, Siberia 12 0.293 -0.353 - DOM W Europe 53 0.526 -2.058* 5.464 (3.998~6.089) 0.00891* 95,900 23,900 12,000 Abbreviations: N, number of samples; SSD, sum of squares deviation. N, Pi, and Tajima's D values were calculated using DNASP v5 and Tau and SSD values were obtained using Arlequin. *P < 0.05, **P < 0.01. a

b Tallinn Tomsk Moscow Novosibirsk Okha a Irkutsk Gorno-Altaysk Mohe Weidesgrun a Komsomolsk-on-Amure Aktobe Chita Birakan Lhotka Kubelhof b Ungheni Astrakhan b 1 Yuzhno-Sakhalinsk a Donetsk Tacheng Hulin Aosta a a Manzhouli c 1 Ljublana W Balkhash L. Bole b 1 b General Toshevo b b Manasi Cislago a Ili Toulouse Binasco Sulak b b Urumqi Tongliao Tashkent Urad b b 1 1 Montpellier Altindere Batumi b b Hami c a c Hokkaido b Bukhara b Turfan b b bb Jiayuguan Jixian Tumen Corse Himera Mashhad Aksu b c 1 Kashi Dunhuang b Laiyang c Noshahr b b b Konchon Monastir 3 b Hotan b b c Golmud b c Epanomi Kabul b 4 Leh b Malia 3 3 Honshu Nicosia Islamabad Lhasa Xiaogan ca Ahvaz b b b 1 2 2 1 1 b 4 1 3 Jiangyin Guilin 1 c Okinawa I. Comilla 1 Pachmarhi 1 1 1 1 1 1 Lashio 2 2 Taitung 1 Mandalay Hanoi Pune 1 Bhubaneswar Dakar 1 1 Manila Mysore 1 Coimbatore 1 Peradeniya 1 Colombo 1 SOMALIA

1 1 Lembang Maluku I. 1 1 1 Bogor Bali I. Flores I.

CAS-1 GEN CAS CAS 2-4 NEP

DOM MUS-1 “Clade F” MUS MUS-2 Montpellier Burra

Mohe Okha b 2 c 3 2 3 Komsomolsk-on-Amure Manzhouli 2 3 1 3 2 2 Birakan 2 2 Kabul 2 4 4 3 4 3 4 3 Leh Islamabad c 3 Qiqihar Yuzhno-Sakhalinsk Lahore Jalandhar 2 2 2 2 Hulin 1 2 2 3 2 1 Sahiwal 1 2 Tukuche 1 1 2 3 Kathmandu Nayoro Bikaner Delhi Changchun 3 4 Fukagawa 1 Ghaziabad Takikawa 1 1 Kyowa c 1 Tongliao Setana 1 1 Kushiro Guwahati 1 Tumen c c Vladivostok ac c Naganuma Kraskino c Date Jixian Okushiri I. Pachmarhi Comilla Khasan Hokkaido 1 1 1 Beijing Baodi Kolkata 1 1 Hwacheongun Otsuchi Baengnyeong I. c Sado I. c Pune 1 Bhubaneswar Jinan c 1 Sendai 2 c Laiyang Ganhwa I. c 1 Aizuwakamatsu Suwon Konchon Tsukuba c Kyoto c Coorg 1 Tottori c Busan c c c c Yamaguchi Fujisawa c Miki c Anjo Mysore 1 Fukuoka c c Tokushima 1 Honshu Coimbatore Jiangyin Kyushu Shikoku 1 Shanghai c Izumi 1 1 Peradeniya Colombo 1 c Tanegashima I.

Figure 1 AF074526

AF074525 AF074524 a 0.01 b DOM CAS M. cypriacusM. macedonicus MUS NEP M. spicilegus M. spretus GEN CAS-4 outgroup outgroup: M. macedonicus 0.0010 CAS-3 NEP CAS-1 CAS-2 MUS CAS DOM c MUS 0.01 d CAS-2 BRC3024 India, HI173 Pakistan AF074538 Pakistan CAS-4 HI520 Vietnam +76 bp GEN HS2400 Taiwan CAS-2 CAS-1 CAS-3 HI261 Pakistan AF074532 PakistanAF07453 Pakistan 0.0010 HI187 India HS1467 AF074526 HS1523 HI262 Pakistan AF074525 CAS AF074524 AF074539 Pakistan HI260 Pakistan NEP HI264 Pakistan HI265 Pakistan AF074523 Nepal: Jomos e

0.0010 0.0010

MG3044 Estonia MUS-2 N China f i E Europe ii iii Russia: Irkutsk HS3608 China: Mohe MG671 Russia: Gorno-Altaysk HS3605 Russia: Seibria, Altai mountain U47527 Russia: Komsomolsk on Amure MG3042 Russia: Novosibirsk MG3053 Russia: Komsomolsk on Amure MG3041 HS3612 MUS-2 MUS-1 MG918 MG928

E Europe U47525 MG3065 HS1413 iv N China HS3612 MUS-1b HS3948 Czech HS1407 HS4333 HS1337 Ukraine vii Korea v Primorye HS1413 vi U047530 Japan

MUS-1 MUS-1c HS1337 E Europe MUS-1a g HG5 HG11 HG4 DOM h 0.0010 HG10 DOM HG3 “Clade F” HG2/1 HG11 MG509 China HG9 MG566 China HG8 0.0010 HG9 HS2322 Indonesia HG10 HS3700 Somalia HG7 HG3

HG9 HG2

HG8 HG9 HG1/2

“Clade F” HG1 HG11 HG6

Figure 2 a Mus spretus Mus macedonicus Mus spicilegus b 99

98 DOM

100

100 NEP 100 CAS

0 DOM

100

MUS

100 98 100

95

90 9082 NEP

90

9797 0.02 MUS

98

90 95

91 CAS

86 0.01 86 GEN 94

Figure 3 Mus macedonicus BRC3021 India: Bikaner 100/100/93 CAS-3 76/58/55 HI161 India: Leh BRC3025 India: Ghaziabad CAS-4 79/76/54 89/89/89 HI302 India: Bhubaneswar MG712 China: Hainan I. CAS CAS-1 100/100/100 100/ HS3357 Myanmar: Lashio 100/ 100 MG834 China: Hulin BRC3024 India: Jalandhar CAS-2 97/93/95 HI187 India: Delhi HS1337 Russia: Khasan HS1413 Russia: Kraskino 71/76/93 HS3612 Russia: Astrakhan HS4233 Korea: Hwacheon-gun MUS-1 HS4412 Japan: Fukuoka 100/96/100 MG992 China: Qiqihar 83/69/68 MUS HS1338 Uzbekistan: Tashkent HS1464 Kazakhstan: Aktobe HS3605 Russia: Gorno-Altaysk 74/69/68 MUS-2 HS3608 Russia: Irkutsk 91/91/97 MG963 China: Laiyang 85/76/96 MG966 China: Laiyang

100/100/100 HS1466 Russia: Komsomolsk 82/63/55 HS3607 Russia: Sakhalin, Okha HS589 Italy: Aosta 100/100/100 DOM HS3604 Russia: Tomsk NIG934 Iran: Ahvaz 86/79/89 MG395 Italy: Binasco HS1467 Nepal: Tukuche NEP 100/100/100 HS1523 Nepal: Kathmandu 0.005 substitutions/site

Figure 4 a CAS-1a Hokkaido MG488 HS2324 HS2326 MG489 Hokkaido HS2445 HS2454 HS506 CAS-1 HS2446 HS2456 HS508 HS1946 HS509 Kunming HS2402 Guilin HS512 Java (Bogor) HI111 Hainan I. MG501N Honshu Bali HI116 MG712 Flores HS3736 MG3047 HI302 S Sakhalin Maluku HS4112 MG863 MG834 Sri Lanka HI481 N China: Manzhouli, Hulin MG504 S China Bangladesh HS3701 MG3046 S Sakhalin BRC3018 HS2925 MG3023 Primorye India HS3721 MG654 MG3077 Bangladesh 0.001 HI134 E Myanmar HS3720 MG438S China MG503 BRC3026 Java (Lembang)

India HI186 W Myanmar BRC3015 S China HS3357 S China CAS-1b

India: Delhi

E Myanmar HI196 Philippines CAS-2 (BRC3024) MG786 S China b MUS-1b

China: Tongliao

MG812 China: Aksu 0.001 Russia: Sulak China: Hulin MG608 CAS (HI481) HS4327 China: Hulin

MG920 China: Hohhot China: MG835China: Turfan Czech: Lhotka MG875

HS3948 MG851

MUS-1c Uzbekistan: Buchara Siberia HS4333 HS4412*MG682** MG3041 MG3042HS3605 HS3608 HS2788**

HS4097** China: Lhasa Korea* MG723 MG4235* Kazakhstan: Aktobe Japan** HS4233* HS1464 China: Laiyang HS4234* China: Manasi MG966 HS4238* MG444* MG597 Uzbekistan: Tashkent China: Laiyang MG980 Russia: Astrakhan China: Tumen HS1338 MG963 MG992 Russia: Kraskino HS4271** MG918 HS3612 China: Hulin

HS1413 China: Qiqihar MG928

HS4325 Moldova China: ZhengZhou MG3065 MUS-2 Ukraine: Donetsk

HS1337 Primorye: Khasan MUS-1 MUS-1a 75-bp duplication

Figure 5 Mus spicilegus AB125775* Mus macedonicus AB125770* Mus cypriacus FR751074* 0.914 MG806 China Jixian 0.464 MG963 China Laiyang MG969 China Laiyang 0.037 MG967 China Laiyang MG968 China Laiyang MG966 China Laiyang 0.072 MG964 China Laiyang HS1338 Uzbekistan Tashkent MUS-2 HS3608 Russia Irkutsk HS3605 Russia GornoAltaysk HS1464 Kazakhstan Aktobe MG597 China Manasi MG869 China Golmud MG870 China Golmud HS3951 Bulgaria Toshevo HS3612 Russia Astrakhan HS1413 Russia Primorye HS4325 Moldova Ungeni HS4326 Moldova Ungeni HS1337 Russia Primorye MG971 China Shijiazhuang MG918 China Hulin MG928 China Zhengzhou MG805 China Baodi MG978 China Shijiazhuang MG956 China Xiaogan MG919 China Hulin HS4327 Russia Sulak MG808 China Hohhot HS4056 Japan Kanagawa Fujisawa E HS4235 Korea Hwacheongun BRC3515 Japan Kagoshima Izumi HS4412 Japan Fukuoka 0.151 HS4275 Japan Yamaguchi HS4273 Japan Yamaguchi HS4274 Japan Yamaguchi MOA Japan Aichi Anjo HS4169 Japan Ibaraki Tsukuba HS4121 Japan Tokushima HS4120 Japan Tokushima AB205274* HS2320 Korea Suwon MG5018 Korea Suwon MG5037 Korea Suwon MG5017 Korea Suwon MUS HS4238 Korea GanghwaIs 1.207 SWNMs Korea Suwon HS4233 Korea Hwacheongun MUS-1 HS4234 Korea Hwacheongun HS1473 Russia Kraskino 0.056 HS4272 Japan Fukuoka HS2788 Japan Okinawa Is HS4246 Japan Sado Is HS4099 Japan Tottori MG422 Japan Kyoto HS682 Korea Baengnyeong Is HS2468 Japan Chiba MG992 China Qiqihar 0.110 HS4057 Japan Kanagwa Fujisawa HS4097 JapanTottori HS4098 Japan Tottori HS4055 Japan Kanagawa Fujisawa AB205317* HS2815 Japan Ishikawa MG0444 Korea Busan HS298 Japan Hokkaido Okushiri Is HS4271 Japan Hokkaido Setana B HS4058 Japan Kanagawa Fujisawa 0.418 HS4411 Japan Hokkaido Setana HS4059 Japan Kanagawa Fujisawa HS4331 Uzbekistan Bukhara YGA_05 Japan Yamagata Sakata HS4333 Uzbekistan Bukhara MG970 China Laiyang MG3044 Estonia Tallinn MG812 China Tongliao MG920 China Hulin MG851 ChinaHohhot MG871 China Dunhuang MG927 China Zhengzhou 0.092 MG5086 China Jiayuguan MG5066 China Beijing MG991 China Qiqihar MG867China Turfan MG608 China Aksu BRC3566 Afghanistan Kabul MG874 China Turfan MG875 China Turfan 0.134 HI161 India Leh HI159 India Leh CAS-3 HI175 Pakistan Islamabad HI484 Sri Lanka Peradeniya BRC3016 India Pune CAS-4 HI302 India Bhubaneswar MG712 China Hainan Is HS506 China Kunming 0.178 HS508 China Kunming A HS2324 Japan Hokkaido Nayoro IWT-01 Japan Iwate Otsuchi HS507 China Kunming AB205276* HS2401 Bogor 0.459 HQ270434* Morocco 0.071 BRC3528 Philippines Quezon CAS-1 CAS HI488 Sri Lanka Colombo HS4112 Indonesia Maluku BRC3017 India Kolkata HS3357 Myanmar Lashio HS4173 India Mysore 1.70 0.217 HI481 Sri Lanka Peradeniya HI485 Sri Lanka Colombo HI483 Sri Lanka Peradeniya HS2340 Japan Hokkaido Otaru D HS2924 Bangladesh Comilla 0.113 MG863 China Manzhouli HI187 India Delhi HS2400 Taiwan Taitung CAS-2 HS1467 Nepal Tukuche HS1523 Nepal Kathmandu HS589 Italy Aosta NEP 0.141 HQ270447* Cyprus HQ270444* Cyprus BFM2Ms France Montpellier G WLA France Toulouse MG411 France Montpellier MG393 Tunisia Monastir HQ270446* Cyprus HQ270440* Italy Zanica WMP Tunisia Monastir HS4303 Greece Crete Malia HS4304 Greece Crete Nidas 0.372 0.088 HQ270455* Cyprus BRC3647 Peru Coppeck HS3882 Philippines Manila 0.100 HQ270450* Senegal Daka r C HS4376 Cyprus Agios HS4372 Cyprus Agios HQ270445* Cyprus HQ270443* Cyprus HS4374 Cyprus Nicosia HS4378 Turkey Altindere HS4379 Turkey Altindere 0.133 HS1466 Russia Komsomolsk HS3607 Russia Sakhalin HQ270439* Tunisia Sfrax ANWCM29995 Australia Burra F HQ270436* Morocco HQ270438* Tunisia DOM HQ270437* Morocco HS3958 Germany Weidesgrun ANWCM29996 Australia Burra MZB22299 Indonesia Bogor PGN Canada Pegion . MG414 Canada Rocheleau HS2322 I ndonesia Bogor HS4302 Greece Crete Malia HQ270451* Iran Habhas HS4317 Greece Epanomi MG395 Italy Binasco 0.116 HQ270448* Iran Hamedon HQ270449* Iran Ahvaz HQ270442* Cyprus MG3055 Russia Moscow HQ270435* Morocco HQ270454* Syria Lattakia 0.078 HS3959 Germany Kubelhof HQ270453* Canary Is HS3604 Russia Tomsk HQ270441* Georgia Adjaria HS4301 Italy Sicily Imera NIG934 Iran Ahvaz HQ270452* Canary Is Mus spretus AB033700*

0.0 0.25 0.5 0.75 1.0 1.25 1.5 1.75

Fig. 6