Tuesday, March 17, 2015

A recent bottleneck of Y chromosome diversity coincides with a global change in culture

I'm super excited to share our new paper, out in Advanced Access in Genome Research, A recent bottleneck of Y chromosome diversity coincides with a global change in culture!

Update: you can listen to a local NPR interview with Mark Brodie about this work here: http://kjzz.org/content/116152/does-evolution-favor-rich-and-powerful

In a nutshell:

Graphic designed by Sabine Deviche.

To help explain the paper, check out this ASUnews article by Sandra Leander: https://asunews.asu.edu/20150316-y-chromosome-bottleneck

And, for a longer, visual, explanation, check out this *awesome* infographic made for us by Sabine Deviche.

Graphic designed by Sabine Deviche.
One on the methods we use to study the Y chromosome and mtDNA is the coalescent. Here is a short video explaining the coalescent, and highlighting the difference between census population size (all the people in the population, and the effective population size (those people who left genetic relics in our DNA that we can study today):


A recent bottleneck of Y chromosome diversity coincides with a global change in culture

    • Monika Karmin*
    • Lauri Saag*
    • Mário Vicente*
    • Melissa A. Wilson Sayres*
    • Mari Järve
    • Ulvi Gerst Talas
    • Siiri Rootsi
    • Anne-Mai Ilumäe
    • Reedik Mägi
    • Mario Mitt
    • Luca Pagani
    • Tarmo Puurand
    • Zuzana Faltyskova
    • Florian Clemente
    • Alexia Cardona
    • Ene Metspalu
    • Hovhannes Sahakyan
    • Bayazit Yunusbayev
    • Georgi Hudjashov
    • Michael DeGiorgio
    • Eva-Liis Loogväli
    • Christina Eichstaedt
    • Mikk Eelmets
    • Gyaneshwer Chaubey
    • Kristiina Tambets
    • Sergei Litvinov
    • Maru Mormina
    • Yali Xue
    • Qasim Ayub
    • Grigor Zoraqi
    • Thorfinn Sand Korneliussen
    • Farida Akhatova
    • Joseph Lachance
    • Sarah Tishkoff
    • Kuvat Momynaliev
    • François-Xavier Ricaut
    • Pradiptajati Kusuma
    • Harilanto Razafindrazaka
    • Denis Pierron
    • Murray P. Cox
    • Gazi Nurun Nahar Sultana
    • Rane Willerslev
    • Craig Muller
    • Michael Westaway
    • David Lambert
    • Vedrana Skaro
    • Lejla Kovačević
    • Shahlo Turdikulova
    • Dilbar Dalimova
    • Rita Khusainova
    • Natalya Trofimova
    • Vita Akhmetova
    • Irina Khidiyatova
    • Daria V. Lichman
    • Jainagul Isakova
    • Elvira Pocheshkhova
    • Zhaxylyk Sabitov
    • Nikolay A. Barashkov
    • Pagbajabyn Nymadawa
    • Evelin Mihailov
    • Joseph Wee Tien Seng
    • Irina Evseeva
    • Andrea Bamberg Migliano
    • Syafiq Abdullah
    • George Andriadze
    • Dragan Primorac
    • Lubov Atramentova
    • Olga Utevska
    • Levon Yepiskoposyan
    • Damir Marjanović
    • Alena Kushniarevich
    • Doron M. Behar
    • Christian Gilissen
    • Lisenka Vissers
    • Joris A. Veltman
    • Elena Balanovska
    • Miroslava Derenko
    • Boris Malyarchuk
    • Andres Metspalu
    • Sardana Fedorova
    • Anders Eriksson
    • Andrea Manica
    • Fernando L. Mendez
    • Tatiana M. Karafet
    • Krishna R. Veeramah
    • Neil Bradman
    • Michael F. Hammer
    • Ludmila P. Osipova
    • Oleg Balanovsky
    • Elza K. Khusnutdinova
    • Knut Johnsen
    • Maido Remm
    • Mark G. Thomas
    • Chris Tyler-Smith
    • Peter A. Underhill
    • Eske Willerslev
    • Rasmus Nielsen
    • Mait Metspalu*
    • Richard Villems*
    • and Toomas Kivisild*

  1. 1Estonian Biocentre, Tartu, 51010, Estonia;
  2. 2Department of Evolutionary Biology, Institute of Molecular and Cell Biology, University of Tartu, Tartu, 51010, Estonia;
  3. 3Department of Botany, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, 51010, Estonia;
  4. 4Division of Biological Anthropology, University of Cambridge, Cambridge, United Kingdom;
  5. 5Department of Integrative Biology, University of California Berkeley, Berkeley, California, USA;
  6. 6School of Life Sciences and The Biodesign Institute, Tempe, Arizona, USA;
  7. 7Department of Bioinformatics, Institute of Molecular and Cell Biology, University of Tartu, Tartu, 51010, Estonia;
  8. 8Estonian Genome Center, University of Tartu, Tartu, 51010, Estonia;
  9. 9Department of Biotechnology, Institute of Molecular and Cell Biology, University of Tartu, Tartu, 51010, Estonia;
  10. 10Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences, Yerevan, Armenia;
  11. 11Institute of Biochemistry and Genetics, Ufa Scientific Center of the Russian Academy of Sciences, Ufa, Russia;
  12. 12Department of Psychology, University of Auckland, Auckland, 1142, New Zealand;
  13. 13Department of Biology, Pennsylvania State University, University Park, Pennsylvania, USA;
  14. 14Department of Applied Social Sciences, University of Winchester, Winchester, United Kingdom;
  15. 15The Wellcome Trust Sanger Institute, Hinxton, United Kingdom;
  16. 16Center of Molecular Diagnosis and Genetic Research, University Hospital of Obstetrics and Gynecology, Tirana, Albania;
  17. 17Center for GeoGenetics, University of Copenhagen, Copenhagen, Denmark;
  18. 18Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia;
  19. 19Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, Russia;
  20. 20Department of Genetics, University of Pennsylvania, Philadelphia, Pennsylvania, USA;
  21. 21School of Biology, Georgia Institute of Technology, Atlanta, Georgia, USA;
  22. 22Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, USA;
  23. 23DNcode Laboratories, Moscow, Russia;
  24. 24Evolutionary Medicine Group, Laboratoire d'Anthropologie Moléculaire et Imagerie de Synthèse, Centre National de la Recherche Scientifique, Université de Toulouse 3, Toulouse, France;
  25. 25Eijkman Institute for Molecular Biology, Jakarta, Indonesia;
  26. 26Statistics and Bioinformatics Group, Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand;
  27. 27Centre for Advanced Research in Sciences (CARS), DNA Sequencing Research Laboratory, University of Dhaka, Dhaka, Bangladesh;
  28. 28Arctic Research Centre, Aarhus University, Aarhus, DK-8000, Denmark;
  29. 29Environmental Futures Research Institute, Griffith University, Nathan, Australia;
  30. 30Genos, DNA Laboratory, Zagreb, Croatia;
  31. 31University of Osijek, Medical School, Osijek, Croatia;
  32. 32Centogene AG, Rostock, Germany;
  33. 33Institute of Bioorganic Chemistry, Academy of Science, Tashkent, 100143, Uzbekistan;
  34. 34Institute of Cytology and Genetics, Novosibirsk, Russia;
  35. 35Institute of Molecular Biology and Medicine, Bishkek, Kyrgyzstan;
  36. 36Kuban State Medical University, Krasnodar, Russia;
  37. 37L. N. Gumilyov Eurasian National University, Astana, Kazakhstan;
  38. 38Center for Life Sciences, Nazarbayev University, Astana, Kazakhstan;
  39. 39Department of Molecular Genetics, Yakut Scientific Centre of Complex Medical Problems, Yakutsk, Russia;
  40. 40Laboratory of Molecular Biology, Institute of Natural Sciences, M. K. Ammosov North-Eastern Federal University, Yakutsk, Russia;
  41. 41Mongolian Academy of Medical Sciences, Ulaanbaatar, Mongolia;
  42. 42National Cancer Centre Singapore, Singapore;
  43. 43Northern State Medical University, Arkhangelsk, Russia;
  44. 44Anthony Nolan, London, UK;
  45. 45Department of Anthropology, University College London, London, United Kingdom;
  46. 46RIPAS Hospital, Bandar Seri Begawan, Brunei;
  47. 47Scientific-Research Center of the Caucasian Ethnic Groups, St. Andrews Georgian University, Tbilisi, Georgia;
  48. 48St. Catherine Specialty Hospital, Zabok, Croatia;
  49. 49Eberly College of Science, Pennsylvania State University, University Park, Pennsylvania, USA;
  50. 50University of Split, Medical School, Split, Croatia;
  51. 51V. N. Karazin Kharkiv National University, Kharkiv, Ukraine;
  52. 52Department of Genetics and Bioengineering, Faculty of Engineering and Information Technologies, International Burch University, Sarajevo, Bosnia and Herzegovina;
  53. 53Institute of Genetics and Cytology, National Academy of Sciences, Minsk, Belarus;
  54. 54Department of Human Genetics, Radboud University Medical Center, Nijmegen, Netherlands;
  55. 55Research Centre for Medical Genetics, Russian Academy of Sciences, Moscow, Russia;
  56. 56Genetics Laboratory, Institute of Biological Problems of the North, Russian Academy of Sciences, Magadan, Russia;
  57. 57Department of Zoology, University of Cambridge, Cambridge, United Kingdom;
  58. 58Integrative Systems Biology Lab, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia;
  59. 59Department of Genetics, Stanford University School of Medicine, Stanford, California, USA;
  60. 60ARL Division of Biotechnology, University of Arizona, Tucson, Arizona, USA;
  61. 61Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York, USA;
  62. 62The Henry Stewart Group, London, United Kingdom;
  63. 63Vavilov Institute for General Genetics, Russian Academy of Sciences, Moscow, Russia;
  64. 64University Hospital of North Norway, Tromsøe, Norway;
  65. 65Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom;
  66. 66Estonian Academy of Sciences, Tallinn, Estonia
  1. Corresponding authors: tk331@cam.ac.ukmonika.karmin@gmail.com
  1. * These authors contributed equally to this work.

Abstract

It is commonly thought that human genetic diversity in non-African populations was shaped primarily by an out-of-Africa dispersal 50–100 thousand yr ago (kya). Here, we present a study of 456 geographically diverse high-coverage Y chromosome sequences, including 299 newly reported samples. Applying ancient DNA calibration, we date the Y-chromosomal most recent common ancestor (MRCA) in Africa at 254 (95% CI 192–307) kya and detect a cluster of major non-African founder haplogroups in a narrow time interval at 47–52 kya, consistent with a rapid initial colonization model of Eurasia and Oceania after the out-of-Africa bottleneck. In contrast to demographic reconstructions based on mtDNA, we infer a second strong bottleneck in Y-chromosome lineages dating to the last 10 ky. We hypothesize that this bottleneck is caused by cultural changes affecting variance of reproductive success among males.


-------------------------------------
Update: Popular Science articles about this research:

Francie Diep, science journalist, Pacific Stand
http://www.psmag.com/nature-and-technology/17-to-1-reproductive-success

Danielle Paquette, Washington Post
http://www.washingtonpost.com/blogs/wonkblog/wp/2015/03/18/how-wealth-trumped-natural-selection-and-changed-our-ancestors-sex-lives/?hpid=z4

Mark Brodie, KJZZ, NPR radio
http://kjzz.org/content/116152/does-evolution-favor-rich-and-powerful

Estonian paper
http://pluss.postimees.ee/3131333/geenid-naitavad-urgmeeste-voimu

Amanda Marcotte, Slate:
http://www.slate.com/blogs/xx_factor/2015/03/20/the_brutality_of_the_stone_age_only_1_man_had_children_for_every_17_women.html?wpsrc=fol_fb

Janet Feng, IFLS
http://www.iflscience.com/health-and-medicine/women-were-out-reproducing-men-4000-years-ago

reddit
http://www.reddit.com/r/science/comments/2zcudp/wealth_and_power_may_have_played_a_stronger_role/

Genetic Engineering and Biotechnology News
http://www.genengnews.com/gen-news-highlights/male-genes-preserve-survival-of-the-wealthiest-legacy/81251045/

Sarah Kaplan, Washington Post
http://www.washingtonpost.com/news/morning-mix/wp/2015/03/18/how-survival-of-the-fittest-became-survival-of-the-richest/

IANS, The Economic Times
http://economictimes.indiatimes.com/magazines/panache/wealth-behind-decline-in-number-of-reproducing-males-study/articleshow/46609782.cms

Will Parker, Science GoGo
http://www.scienceagogo.com/news/20150216195902.shtml

ANI, ZeeNewsIndia
http://zeenews.india.com/news/sci-tech/male-genetic-diversity-declined-due-to-wealth-power-rather-than-survival-of-fittest_1563084.html

News Staff, Science2.0
http://www.science20.com/news_articles/social_fitness_did_a_genetic_bottleneck_occur_because_of_wealth_and_power-154047

Anthony Rivas, Medical Daily
http://www.medicaldaily.com/did-cultural-shift-influence-human-evolution-how-farming-might-have-changed-genetic-326094



14 comments:

Kirk Maxey said...

It's interesting that your leading hypothesis for the inability of 16/17 of the males to reproduce was poverty. Is it not more likely that they were organized into armies to protect the newly amassed stores of grain and animals that agriculture brought? Thus engaged, they were likely to be killed at an early age, and also to be far afield and out of contact with their wives if they even had one. Those men fathering all the children might not have been the strongest or the wealthiest, but just the ones who could produce some excuse to stay behind with the women and out of the battles. So, survival of the weaseliest. :-)

mathbionerd said...

I'm actually about to talk to more anthropologists soon, to ask more about this very topic. Thanks for sharing your ideas! I'm really curious to learn what other disciplines have to say about our findings.

Anonymous said...

So what ended the bottleneck 4000 years ago?

The idea that agriculture was responsible seems far too pat. Agriculture began 2000 years earlier than the bottleneck and continues to the present day.

The rise of agrarian civilization was staggered, with separate developments in the fertile crescent, China, and the Americas. So why aren't there three staggered bottlenecks?

mathbionerd said...

Very good points.

1. We don't know exactly what allowed the recovery. Still need more work on this.

2. We don't think it was agriculture itself, but accumulation of wealth after agriculture.

3. Absolutely, agriculture was staggered and in figure 2 in our manuscript, we actually show that there were different dips in different parts of the world, where the timing of the dips ranges between 4000 to 8000 years ago.

http://genome.cshlp.org/content/early/2015/03/13/gr.186684.114.abstract

Anonymous said...

I can't view Figure 2 as it's paywalled. Figure S4B breaks down by region but doesn't seem to show the ratio, S5 shows the Nf/Nm ratio but only in aggregate.

SON948 said...

Dr. Sayres -- Did you really say this?

“Instead of ‘survival of the fittest’ in a biological sense, the accumulation of wealth and power may have increased the reproductive success of a limited number of ‘socially fit’ males and their sons,” said Melissa Wilson Sayres"

Or is this an egregious mis-quote by an unprincipled would-be journalist?

...because it is completely wrong.

Just curious...

Tomenable said...
This comment has been removed by the author.
Tomenable said...

Really interesting reading, thank you very much!

That bottleneck of Y-DNA lineages seems to coincide quite well in time with the invasion of Europe by Proto-Indo-Europeans (ca. 5000 years ago), who apparently brought with them R1a and R1b haplogroups of Y-DNA. Some recent papers about this:

"Massive migration from the steppe is a source for Indo-European languages in Europe":

http://biorxiv.org/content/biorxiv/early/2015/02/10/013433.full.pdf

www.cell.com/current-biology/abstract/S0960-9822%2809%2901694-7?cc=y

http://www.nature.com/ncomms/2013/131001/ncomms3486/full/ncomms3486.html

http://biorxiv.org/content/biorxiv/early/2015/03/13/016477.full.pdf

"Peopling of Europe – Identifying the Ghost Population":

http://dna-explained.com/2014/10/21/peopling-of-europe-2014-identifying-the-ghost-population/

"Michael Hammer – Origins of R1b Haplogroup Diversity in Europe":

http://dna-explained.com/2013/11/12/2013-family-tree-dna-conference-day-2/

"Mike Hammer goes for post-Neolithic entry of R lineages into Europe":

http://www.anthrogenica.com/showthread.php?1577-Mike-Hammer-goes-for-post-Neolithic-entry-of-R-into-Europe

Tomenable said...

And this documentary explains, that those could well be Indo-European newcomers who caused that change in culture, and that all those innovations they brough with them (metal weapons, smelting technology, wheleed vehicles, horses, domesticated animals, less reliance on agriculture and more on dairy / milk; precious trade goods and rare skills) perhaps conferred reproductive advantage to them (as well as helped them to get wealthy - which further conferred even more reproductive advantage to those Indo-European males of R1b and R1a haplogroups):

"Indo-Europeans in Northern Europe" documentary:

Part 1:

https://www.youtube.com/watch?v=hmHXBXG7Loo

Part 2:

https://www.youtube.com/watch?v=XNNePv5Hu5Y

Tomenable said...

PIE cultures and societies were extremely patriarchal, as explained in this video:

https://www.youtube.com/watch?v=ErXa5PyHj4I

In contrast to matriarchal societies of Neolithic farmers, such as Trypillian culture:

https://www.youtube.com/watch?v=l6IgYxfTYTg


David Brin said...

Agriculture is physically very arduous, requiring more persistent use of strength (as opposed to agility and endurance) in order to achieve results. Also a relentlessness of labor that would tax any animal or hunter-gatherer.

This suggests either (1) a great advantage to those who could do this... or (2) a great advantage to those who could control the males who could do this... or both.

There are aspects that go unmentioned. Among mammals, there is a relationship between male-female size differential and the species' average mating ratio across lifespan. Almost-monogamous species show little size difference. Elephant seals and elk are very dimorphic, reflecting very large (though temporary) harem size.

(Note alpha bulls wear themselves out and seldom last long. This is not a cushy way of life.)

The ratio for humans has long been known to fit this curve at a 1.3 scale, meaning that about one-third of human males would be expected to have an extra wife. (in parallel or serially). This just happens to fit the pattern seen in a majority of human tribes and nations of the past. (Note that this polygamy was sometimes run by the women for THEIR benefit, as in the Cherokee and Iroquoisan peoples.)

Hence the question... were there variations in the male-female SIZE ratio dimorphism, during this bottleneck? It would seem to be a natural thing to look for, in correlation with this study.

David Brin
Author of EARTH and The Transparent Society

David Brin said...

PS I will be speaking near ASU April 16-18.
http://cofes.com/Events/COFES-2015/Agenda.aspx

mathbionerd said...

Thanks for all the discussion, everyone. I hope this is one post, where readers will take time to read through the comments.

The article is paywalled for six months, but if you email me, I can send you the proof.

David Brin said...

How doth one email thou? From your Mathbionerd page, I cannot even discover your NAME!

Please do send a reprint to davidbrin@sbcglobal.net