Seeing genes in space & time: the evolution of neutral and functional genetic diversity using woolly mammoth

Lead Research Organisation: The Natural History Museum
Department Name: Earth Sciences

Abstract

Understanding how a population changes through time is critical to understanding the broader picture of species evolution and extinction. By examining the dynamics of population change, we can explore how, as a result of changing competitive pressures and habitats, species distributions alter through time and space. Populations can increase or decline, or differ in their levels of migration and immigration. Although it is theoretically possible to directly observe these processes, the time span across which observations would be necessary renders this all but impractical. Fortunately, direct observation is not the only way to infer changes occurring in populations, because all of these processes leave traces in the genetic diversity of a species. By sequencing pieces of genetic information of a species (DNA) from a large number of individuals within a population, it is possible to shed light on the dynamics of species going back hundreds of thousands of years.

When analysing data from modern populations, data may be insufficient to acquire the full picture of past population change - any information from populations no longer around today will be lost. A far more powerful approach is to directly sample the genetics of past populations. This approach uses ancient DNA: DNA that survives trapped in tissue such as hair and bone dating back to ~120,000 years. Research in ancient DNA has shown that the dynamics of Pleistocene populations were more complicated than had been initially inferred from modern data alone. Critically, the Pleistocene is a period which covered a series of large changes in climate, and a detailed examination of Pleistocene population dynamics may shed light on how species respond to the effects of climate change.

However, there are difficulties arising from the decay of DNA over time, which leaves relatively few bones that can be successfully sampled, and results in short pieces of DNA, problematic for analyses. One upshot of this is that most ancient DNA studies to date have relied on an abundant, short loop of DNA called mitochondrial (mt) DNA. However, mtDNA is only passed down through the maternal line, and cannot provide any information on the paternal lineage. Sequencing a large number of dated bone samples for longer sequences of both mtDNA, and DNA from the cell nucleus, would shed light on both male and female evolutionary history, and provide a much better insight into how animal populations have changed over the last few hundred thousand years.

The woolly mammoth, an icon for both the Pleistocene and species extinction, is an ideal species in which to study how animals may be affected by climate and environmental change. Moreover, by examining genes that may be favoured during times of climate change, such as those involved in hair growth or cold adaptation, it will be possible to investigate any differing patterns in the DNA between these and more 'neutral' genes, helping us to better understand both the demographic and adaptive processes taking place in these populations.
Recent progress has made such a project possible. Using new high-throughput technologies for analysing DNA, in combination with methods to locate the specific DNA fragments of interest, we can now rapidly and efficiently analyse thousands of units of DNA code from hundreds of fossil remains, allowing us to infer what happened to populations in the past.

Planned Impact

The Potential Economic and Societal Impacts are outlined below; academic impacts are detailed in the Academic Beneficiaries document.

The Public. Supporting a better public understanding of biological evolution is of great importance for our society. The woolly mammoth as both an iconic species and an example of a species of tropical origin that evolutionarily adapted to a completely different environment, provides an excellent possibility to raise interest in evolutionary processes and demonstrate how evolution transforms species over time. The great public interest in mammoths will allow us to reach a broad public, starting from young children to adults of all age groups and educational backgrounds. We will directly engage the public by organizing talks with school children and giving public lectures as detailed in our Pathways to Impact plan and indirectly by writing a popular scientific article in a broadly disseminated magazine. Moreover, research on mammoth, especially genetic analyses as planned in our project, are generally met with great interest by the media and have previously figured heavily in a wide range of magazines, newspapers, online resources and television documentaries (e.g. National Geographic, Financial Times, BBC).

Conservation policy makers. Although gene flow is somewhat on the agenda of conservation policy makers as one factor contributing to the survival of threatened species, the long-term adaptive importance of gene flow is not yet well recognized. However, many Eurasian species have a large geographical distribution, with populations in different habitats likely having differential local adaptations. Therefore, especially during times of environmental change such as the upcoming human-induced climate change, migratory corridors that allow populations to exchange potentially adaptive alleles are likely to play an important role for the long-term survival of species. Showing the importance of such adaptive gene flow for species in the past will give policy makers strong arguments in favour of migratory corridors connecting otherwise isolated protected areas.

Education (schools and museums). Museums and schools will benefit from the research as our results will elucidate the genetic basis of evolution in a popular species. Our results will provide the basic scientific knowledge to better explain how animals adapt to environmental changes and how important it is for the long-term survival of species to have natural, viable populations that can exchange genes rather than only isolated small breeding groups in zoos. As such, our results will have the potential to feature in both museum exhibitions and schools material.

A better understanding of the long-term dynamics of different types of genetic markers as well as the importance of adaptive introgression in evolution will be important for researchers working in Evolutionary biology, Population ecology, Conservation biology and Quaternary science (see Academic Beneficiaries).

Publications

10 25 50
 
Description I have clarified the taxonomy and evolution of mammoths in the northern hemisphere, an essential prerequisite to the interpretation of the molecular (DNA sequence) data being obtained by other members of the team. In particular, I have demonstrated a complex process of species evolution whereby advanced mammoths arose in eastern Asia around 2 million years ago and spread eastwards into N America and westwards into Europe. The North American 'Columbian mammoth' therefore did not evolve in situ over a long period as thought, but was an immigrant. Subsequently the woolly mammoth arose in NE Siberia and likewise spread east and west, and in both cases, in N America and in Europe, met and very probably interbred with the encumbent species. I demonstrated this by morphology and it is strongly confirmed by new DNA evidence from N America. Parallel molecular work on European material is still in progress in our project.

In a 2018 paper (Dickinson et al 2018) we demonstrated a new method of dating mammoth remains that will alllow specimens with DNA but no collagen for radiocarbon to be included in tree-building methods that require dated samples.

In another 2018 paper we obtained the first ancient DNA from subfossil Asian elephants, greatly extending the geographical range and allowing the beginning of the same kind of analysis as we achieved fro mammoth.
Exploitation Route Other groups working on mammoth evolution, both using molecular and morphological data, are using my new taxonomic framework as a benchmark. Other researchers looking at speciation in the fossil record will find this one of the most advanced case-studies available. The new taxonomy is altering the ways museums are curating their mammoth fossils and explaining them to the public.
Sectors Education,Culture, Heritage, Museums and Collections

URL http://www.livescience.com/52785-north-american-mammoths.html
 
Description There was considerable media coverage of several of the outputs, especially the 2015 Science paper on mammoth evolution. See, for example, NHM website (http://www.nhm.ac.uk/our-science/science-news/2015/november/north-american-mammoth-origins-rewritten.html), and LiveScience independent website (http://www.livescience.com/52785-north-american-mammoths.html) and even a Physics website (http://phys.org/news/2015-11-closer-teeth-columbian-mammoth-eurasian.html)
First Year Of Impact 2015
Sector Education,Culture, Heritage, Museums and Collections
Impact Types Cultural

 
Description Mammoths: Ice Age Giants 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I was chief scientific advisor to the Natural History Museum's exhibition 'Mammoths: Ice Age Giants', and made sure outputs from our funded research were included in the exhibition.

126,000 visitors saw the exhibition. I also did numerous media activities, special tours, etc.
Year(s) Of Engagement Activity 2014
URL http://www.nhm.ac.uk/about-us/news/2014/may/emotional-welcome-for-beautiful-mammoth-lyuba130851.html
 
Description Talk on Natural History of Mammoth to Amateur Geological Society, 14th June 2016 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Talk to local geological society. Sparked discussion afterwards.
Year(s) Of Engagement Activity 2016
URL https://amgeosoc.wordpress.com/meeting-dates/
 
Description Talk on mammoths at the Shropshire Hills Discovery Centre, 8th October 2016 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Keynote talk as part of activity weekend across Shropshire to celebrate 30 years since the excavation of the Shropshire mammoths (which I co-led). Update on the research done since that date and ongoing. Generated great interest and much discussion, as well as renewed local pride.
Year(s) Of Engagement Activity 2016
URL http://www.shropshirestar.com/entertainment/2016/09/14/mammoth-weekend-at-shropshire-hills-discovery...
 
Description Talk to students at the Lyell Society, Royal Holloway, 25th February 2016 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Undergraduate students
Results and Impact Invited talk on Late Quaternary Extinctions to geology students at Royal Holloway. Sparked questions and discussion afterwards.
Year(s) Of Engagement Activity 2016