Multiple migrations to the Philippines during the last 50,000 years

doi:10.1073/pnas.2026132118

. 2021 Mar 30;118(13):e2026132118.

doi: 10.1073/pnas.2026132118.

Multiple migrations to the Philippines during the last 50,000 years

Maximilian Larena¹, Federico Sanchez-Quinto^{2

3}, Per Sjödin², James McKenna², Carlo Ebeo^{4

5}, Rebecca Reyes^{6

7}, Ophelia Casel⁸, Jin-Yuan Huang⁹, Kim Pullupul Hagada^{7

10}, Dennis Guilay¹¹, Jennelyn Reyes¹², Fatima Pir Allian^{13

14}, Virgilio Mori¹⁴, Lahaina Sue Azarcon¹⁵, Alma Manera¹⁶, Celito Terando^{17

18}, Lucio Jamero Jr⁶, Gauden Sireg^{19

20}, Renefe Manginsay-Tremedal²⁰, Maria Shiela Labos^{21

22}, Richard Dian Vilar^{23

24}, Acram Latiph²⁵, Rodelio Linsahay Saway²⁶, Erwin Marte²⁷, Pablito Magbanua^{7

28}, Amor Morales²⁹, Ismael Java^{30

31}, Rudy Reveche^{31

32}, Becky Barrios^{33

34}, Erlinda Burton³⁵, Jesus Christopher Salon^{35

36}, Ma Junaliah Tuazon Kels², Adrian Albano^{37

38}, Rose Beatrix Cruz-Angeles³⁹, Edison Molanida^{39

40}, Lena Granehäll², Mário Vicente², Hanna Edlund², Jun-Hun Loo⁹, Jean Trejaut⁹, Simon Y W Ho⁴¹, Lawrence Reid^{5

42}, Helena Malmström^{2

43}, Carina Schlebusch^{2

43

44}, Kurt Lambeck⁴⁵, Phillip Endicott⁴⁶, Mattias Jakobsson^{1

43

44}

Affiliations

¹ Human Evolution, Department of Organismal Biology, Uppsala University, SE-752 36 Uppsala, Sweden; maximilian.larena@ebc.uu.se kurt.lambeck@anu.edu.au mattias.jakobsson@ebc.uu.se.
² Human Evolution, Department of Organismal Biology, Uppsala University, SE-752 36 Uppsala, Sweden.
³ Instituto Nacional de Medicina Genómica, 14610 Mexico City, Mexico.
⁴ National Committee on Cultural Education, National Commission for Culture and the Arts, Intramuros, Manila, 1002 Metro Manila, Philippines.
⁵ National Museum of the Philippines, Ermita, Manila, 1000 Metro Manila, Philippines.
⁶ Ayta Magbukon Cultural Bearer, Ayta Magbukon Indigenous Cultural Community, Abucay, 2114 Bataan, Philippines.
⁷ National Commission on Indigenous Peoples, 1103 Quezon City, Philippines.
⁸ Mindanao Doctors Hospital and Cancer Center, Kabacan, 9407 Cotabato, Philippines.
⁹ Molecular Anthropology and Transfusion Medicine Research Laboratory, Mackay Memorial Hospital, 10449 Taipei City, Taiwan.
¹⁰ Young Indigenous Peoples Empowered to Act in Community Engagement, Diffun, 3401 Quirino, Philippines.
¹¹ Balangao Indigenous Cultural Community, Paracaelis, 2625 Mountain Province, Cordillera Administrative Region, Philippines.
¹² Department of Education-Bataan Division, 2100 Bataan, Philippines.
¹³ Nisa Ul Haqq fi Bangsamoro, 7000 Zamboanga City, Bangsamoro Autonomous Region in Muslim Mindanao, Philippines.
¹⁴ Tarbilang Foundation, Inc., Bongao, 7500 Tawi-Tawi, Bangsamoro Autonomous Region in Muslim Mindanao, Philippines.
¹⁵ Center for Language and Culture, Quirino State University, Barangay Andres Bonifacio, Diffun, 3401 Quirino, Philippines.
¹⁶ Center for Language and Culture, Cagayan State University-Andrews Campus, Tuguegarao, 3500 Cagayan, Philippines.
¹⁷ Tagakaulo Indigenous Cultural Community, Malungon, 9503 Sarangani, Philippines.
¹⁸ Sulong Tribu Program, Provincial Government of Sarangani, Glan, 9517 Sarangani, Philippines.
¹⁹ Subanen Indigenous Cultural Community, Lakewood, 7014 Zamboanga del Sur, Philippines.
²⁰ Dumendingan Arts Guild Inc., Pagadian City, 7016 Zamboanga del Sur, Philippines.
²¹ Ateneo Institute of Anthropology, Ateneo de Davao University, 8016 Davao City, Philippines.
²² Museo Dabawenyo, Andres Bonifacio Rotunda, Poblacion District, 8000 Davao City, Philippines.
²³ Cultural Outreach Program, Kaliwat Performing Artists Collective, Lanang, 8000 Davao City, Philippines.
²⁴ Culture, Heritage, and Arts Office, Local Government Unit of Butuan, 8600 Butuan City, Philippines.
²⁵ Institute for Peace and Development in Mindanao, Mindanao State University-Marawi Campus, Marawi City, 9700 Lanao del Sur, Bangsamoro Autonomous Region in Muslim Mindanao, Philippines.
²⁶ Talaandig Indigenous Cultural Community, Lantapan, 8722 Bukidnon, Philippines.
²⁷ Legal Affairs Office, Indigenous People's Mandatory Representative-Sangguniang Panlalawigan, 8700 Bukidnon, Northern Mindanao, Philippines.
²⁸ Cuyonon Indigenous Cultural Community, Cuyo Island, 5318 Palawan, Philippines.
²⁹ Surigaonon Heritage Center, Surigao City, 8400 Surigao del Norte, Philippines.
³⁰ Kabankalan City Cultural and Tourism Foundation, Inc, Kabankalan City, 6111 Negros Occidental, Philippines.
³¹ Cultural Research and Documentation, Negros Museum, Bacolod, 6100 Negros Occidental, Philippines.
³² Culture and Arts Program, Colegio San Agustin, Bacolod, 6100 Negros Occidental, Philippines.
³³ Panaghiusa Alang Sa Kaugalingnan Ug Kalingkawasan, Inc., Bunawan, 8506 Agusan del Sur, Philippines.
³⁴ Agusan Manobo Indigenous Cultural Community, La Paz, 8508 Agusan del Sur, Philippines.
³⁵ Museo de Oro, Xavier University-Ateneo de Cagayan, 9000 Cagayan de Oro City, Philippines.
³⁶ City Museum of Cagayan de Oro, 9000 Cagayan de Oro City, Philippines.
³⁷ Kalanguya Indigenous Cultural Community, Tinoc, 3609 Ifugao, Cordillera Administrative Region, Philippines.
³⁸ Office of Tinoc Campus Administrator, Ifugao State University, Tinoc, 3609 Ifugao, Cordillera Administrative Region, Philippines.
³⁹ Heritage Office, National Commission for Culture and the Arts, Intramuros, Manila, 1002 Metro Manila, Philippines.
⁴⁰ Office of the Executive Director, National Commission for Culture and the Arts, Intramuros, 1002 Metro Manila, Manila, Philippines.
⁴¹ School of Life and Environmental Sciences, University of Sydney, Sydney, NSW 2006, Australia.
⁴² Department of Linguistics, University of Hawai'i at Mānoa, Honolulu, HI 96822.
⁴³ Palaeo-Research Institute, University of Johannesburg, Auckland Park, 2006, South Africa.
⁴⁴ SciLifeLab, 75236 Uppsala, Sweden.
⁴⁵ Research School of Earth Sciences, The Australian National University, ACT 0200, Canberra, Australia; maximilian.larena@ebc.uu.se kurt.lambeck@anu.edu.au mattias.jakobsson@ebc.uu.se.
⁴⁶ Department Hommes Natures Societies, Musée de l'Homme, 75016 Paris, Ile de France, France.

PMID: 33753512
PMCID: PMC8020671
DOI: 10.1073/pnas.2026132118

Multiple migrations to the Philippines during the last 50,000 years

Maximilian Larena et al. Proc Natl Acad Sci U S A. 2021.

. 2021 Mar 30;118(13):e2026132118.

doi: 10.1073/pnas.2026132118.

Authors

Affiliations

¹ Human Evolution, Department of Organismal Biology, Uppsala University, SE-752 36 Uppsala, Sweden; maximilian.larena@ebc.uu.se kurt.lambeck@anu.edu.au mattias.jakobsson@ebc.uu.se.
² Human Evolution, Department of Organismal Biology, Uppsala University, SE-752 36 Uppsala, Sweden.
³ Instituto Nacional de Medicina Genómica, 14610 Mexico City, Mexico.
⁴ National Committee on Cultural Education, National Commission for Culture and the Arts, Intramuros, Manila, 1002 Metro Manila, Philippines.
⁵ National Museum of the Philippines, Ermita, Manila, 1000 Metro Manila, Philippines.
⁶ Ayta Magbukon Cultural Bearer, Ayta Magbukon Indigenous Cultural Community, Abucay, 2114 Bataan, Philippines.
⁷ National Commission on Indigenous Peoples, 1103 Quezon City, Philippines.
⁸ Mindanao Doctors Hospital and Cancer Center, Kabacan, 9407 Cotabato, Philippines.
⁹ Molecular Anthropology and Transfusion Medicine Research Laboratory, Mackay Memorial Hospital, 10449 Taipei City, Taiwan.
¹⁰ Young Indigenous Peoples Empowered to Act in Community Engagement, Diffun, 3401 Quirino, Philippines.
¹¹ Balangao Indigenous Cultural Community, Paracaelis, 2625 Mountain Province, Cordillera Administrative Region, Philippines.
¹² Department of Education-Bataan Division, 2100 Bataan, Philippines.
¹³ Nisa Ul Haqq fi Bangsamoro, 7000 Zamboanga City, Bangsamoro Autonomous Region in Muslim Mindanao, Philippines.
¹⁴ Tarbilang Foundation, Inc., Bongao, 7500 Tawi-Tawi, Bangsamoro Autonomous Region in Muslim Mindanao, Philippines.
¹⁵ Center for Language and Culture, Quirino State University, Barangay Andres Bonifacio, Diffun, 3401 Quirino, Philippines.
¹⁶ Center for Language and Culture, Cagayan State University-Andrews Campus, Tuguegarao, 3500 Cagayan, Philippines.
¹⁷ Tagakaulo Indigenous Cultural Community, Malungon, 9503 Sarangani, Philippines.
¹⁸ Sulong Tribu Program, Provincial Government of Sarangani, Glan, 9517 Sarangani, Philippines.
¹⁹ Subanen Indigenous Cultural Community, Lakewood, 7014 Zamboanga del Sur, Philippines.
²⁰ Dumendingan Arts Guild Inc., Pagadian City, 7016 Zamboanga del Sur, Philippines.
²¹ Ateneo Institute of Anthropology, Ateneo de Davao University, 8016 Davao City, Philippines.
²² Museo Dabawenyo, Andres Bonifacio Rotunda, Poblacion District, 8000 Davao City, Philippines.
²³ Cultural Outreach Program, Kaliwat Performing Artists Collective, Lanang, 8000 Davao City, Philippines.
²⁴ Culture, Heritage, and Arts Office, Local Government Unit of Butuan, 8600 Butuan City, Philippines.
²⁵ Institute for Peace and Development in Mindanao, Mindanao State University-Marawi Campus, Marawi City, 9700 Lanao del Sur, Bangsamoro Autonomous Region in Muslim Mindanao, Philippines.
²⁶ Talaandig Indigenous Cultural Community, Lantapan, 8722 Bukidnon, Philippines.
²⁷ Legal Affairs Office, Indigenous People's Mandatory Representative-Sangguniang Panlalawigan, 8700 Bukidnon, Northern Mindanao, Philippines.
²⁸ Cuyonon Indigenous Cultural Community, Cuyo Island, 5318 Palawan, Philippines.
²⁹ Surigaonon Heritage Center, Surigao City, 8400 Surigao del Norte, Philippines.
³⁰ Kabankalan City Cultural and Tourism Foundation, Inc, Kabankalan City, 6111 Negros Occidental, Philippines.
³¹ Cultural Research and Documentation, Negros Museum, Bacolod, 6100 Negros Occidental, Philippines.
³² Culture and Arts Program, Colegio San Agustin, Bacolod, 6100 Negros Occidental, Philippines.
³³ Panaghiusa Alang Sa Kaugalingnan Ug Kalingkawasan, Inc., Bunawan, 8506 Agusan del Sur, Philippines.
³⁴ Agusan Manobo Indigenous Cultural Community, La Paz, 8508 Agusan del Sur, Philippines.
³⁵ Museo de Oro, Xavier University-Ateneo de Cagayan, 9000 Cagayan de Oro City, Philippines.
³⁶ City Museum of Cagayan de Oro, 9000 Cagayan de Oro City, Philippines.
³⁷ Kalanguya Indigenous Cultural Community, Tinoc, 3609 Ifugao, Cordillera Administrative Region, Philippines.
³⁸ Office of Tinoc Campus Administrator, Ifugao State University, Tinoc, 3609 Ifugao, Cordillera Administrative Region, Philippines.
³⁹ Heritage Office, National Commission for Culture and the Arts, Intramuros, Manila, 1002 Metro Manila, Philippines.
⁴⁰ Office of the Executive Director, National Commission for Culture and the Arts, Intramuros, 1002 Metro Manila, Manila, Philippines.
⁴¹ School of Life and Environmental Sciences, University of Sydney, Sydney, NSW 2006, Australia.
⁴² Department of Linguistics, University of Hawai'i at Mānoa, Honolulu, HI 96822.
⁴³ Palaeo-Research Institute, University of Johannesburg, Auckland Park, 2006, South Africa.
⁴⁴ SciLifeLab, 75236 Uppsala, Sweden.
⁴⁵ Research School of Earth Sciences, The Australian National University, ACT 0200, Canberra, Australia; maximilian.larena@ebc.uu.se kurt.lambeck@anu.edu.au mattias.jakobsson@ebc.uu.se.
⁴⁶ Department Hommes Natures Societies, Musée de l'Homme, 75016 Paris, Ile de France, France.

PMID: 33753512
PMCID: PMC8020671
DOI: 10.1073/pnas.2026132118

Abstract

Island Southeast Asia has recently produced several surprises regarding human history, but the region's complex demography remains poorly understood. Here, we report ∼2.3 million genotypes from 1,028 individuals representing 115 indigenous Philippine populations and genome-sequence data from two ∼8,000-y-old individuals from Liangdao in the Taiwan Strait. We show that the Philippine islands were populated by at least five waves of human migration: initially by Northern and Southern Negritos (distantly related to Australian and Papuan groups), followed by Manobo, Sama, Papuan, and Cordilleran-related populations. The ancestors of Cordillerans diverged from indigenous peoples of Taiwan at least ∼8,000 y ago, prior to the arrival of paddy field rice agriculture in the Philippines ∼2,500 y ago, where some of their descendants remain to be the least admixed East Asian groups carrying an ancestry shared by all Austronesian-speaking populations. These observations contradict an exclusive "out-of-Taiwan" model of farming-language-people dispersal within the last four millennia for the Philippines and Island Southeast Asia. Sama-related ethnic groups of southwestern Philippines additionally experienced some minimal South Asian gene flow starting ∼1,000 y ago. Lastly, only a few lowlanders, accounting for <1% of all individuals, presented a low level of West Eurasian admixture, indicating a limited genetic legacy of Spanish colonization in the Philippines. Altogether, our findings reveal a multilayered history of the Philippines, which served as a crucial gateway for the movement of people that ultimately changed the genetic landscape of the Asia-Pacific region.

Keywords: Austronesian; ISEA; Negrito; Philippines; human population genetics.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interest.

Figures

**Fig. 1.**
Overview of Philippine population structure. (A) Location of indigenous cultural communities included in the study. The populations are color-coded to represent ethnic group clusters. (B) PCA with worldwide populations, with sample size matched for each regional group. (C) PCA restricted to Philippine ethnic groups. (D) Clustering of Asia-Pacific populations (315,692 SNPs) with an *Inset Graph* showing clustering of 115 Philippine populations (2.3 million SNPs), assuming K number of genetic ancestry components.

**Fig. 2.**
Inferred admixture graph models for Australasians and East Asians. Inferred admixture graph models based on a combination of qpGraph and f statistical analyses presented in *SI Appendix*, Figs. S4–S8. (A) Topology of Australasian cluster indicating pulses of Denisovan introgression events, and estimation of divergence time between Philippine Negritos and AustraloPapuans. (B) Topology of the East Asian cluster showing relationships between Cordillerans, Manobo, Sama, and mainland Asian ethnic groups with inferred admixture events and divergence dates. See main text for divergence time confidence intervals.

**Fig. 3.**
Model for Philippine demographic history. Suggested models for the five major migration events into the Philippines, (A) starting with entry of Northern Negritos and Southern Negritos into the Philippines from Sundaland, (B and C) followed by south-to-north movement of Manobo-related and Sama-related populations during the end of Last Glacial Period, and (D) culminating with the Holocene expansion of Cordilleran-related populations.

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References

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[1] Détroit F., et al. ., A new species of Homo from the Late Pleistocene of the Philippines. Nature 568, 181–186 (2019). - PubMed

[2] Détroit F., et al. ., A new species of Homo from the Late Pleistocene of the Philippines. Nature 568, 181–186 (2019). - PubMed

[3] Mijares A. S., et al. ., New evidence for a 67,000-year-old human presence at Callao Cave, Luzon, Philippines. J. Hum. Evol. 59, 123–132 (2010). - PubMed

[4] Mijares A. S., et al. ., New evidence for a 67,000-year-old human presence at Callao Cave, Luzon, Philippines. J. Hum. Evol. 59, 123–132 (2010). - PubMed

[5] Jinam T. A., et al. ., Discerning the origins of the negritos, first Sundaland people: Deep divergence and archaic admixture. Genome Biol. Evol. 9, 2013–2022 (2017). - PMC - PubMed

[6] Jinam T. A., et al. ., Discerning the origins of the negritos, first Sundaland people: Deep divergence and archaic admixture. Genome Biol. Evol. 9, 2013–2022 (2017). - PMC - PubMed

[7] Reid L. A., Who are the Philippine negritos? Evidence from language. Hum. Biol. 85, 329–358 (2013). - PubMed

[8] Reid L. A., Who are the Philippine negritos? Evidence from language. Hum. Biol. 85, 329–358 (2013). - PubMed

[9] Soares P. A., et al. ., Resolving the ancestry of Austronesian-speaking populations. Hum. Genet. 135, 309–326 (2016). - PMC - PubMed

[10] Soares P. A., et al. ., Resolving the ancestry of Austronesian-speaking populations. Hum. Genet. 135, 309–326 (2016). - PMC - PubMed

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Multiple migrations to the Philippines during the last 50,000 years

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Multiple migrations to the Philippines during the last 50,000 years

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