Deciphering the genomic signatures of speciation and introgression
Lead Research Organisation:
University of Edinburgh
Department Name: Inst of Evolutionary Biology
Abstract
As species diverge, so do their genomes. However, this genetic divergence, which can be measured directly by comparing sequences, has a large random component. Firstly, genetic diversity present within an ancestral species is passed on to its descendants at random and can survive for a long time. Secondly, there may be genetic exchange after the initial split, which further increases the variance in genetic divergence. Being able to model both processes matters in many ways: Firstly, researchers are often want to make inferences about the history of closely related species and ideally identify the factors that caused them to diverge from their genome sequence. For example, it would be interesting to know whether our own ancestors hybridized with Neanderthals in places where they met. Since speciation happens over evolutionary timescales, such indirect inferences from genomic data are often the only way to study the process. Secondly, there is great interest in identifying regions of the genome that may have been under selection both between and within species. In the case of recently diverged species this can tell us which genes were involved in divergence and provides clues about the mechanisms of speciation and the roles of genome structure and geographic separation. Finally, gene flow or introgression between nascent species may be adaptive itself. For example, resistance to insecticide can be acquired more rapidly from close relatives that have already evolved this trait than through independent evolution. To have any hope to identify introgression or selection involving particular genes, we need to know exactly what effects different scenarios of divergence between species have on patterns of neutral diversity in the genome. However, distinguishing between even the simplest histories requires large amounts of data and has proven notoriously difficult. With the rapid advances in sequencing technology, our ability to draw inferences about species divergence is now limited by theory rather than data. I will develop new statistical methods that allow us to estimate key parameters of the divergence between two species, in particular their splitting time and the amount and direction of gene flow between them directly and exactly from genomic data. These methods will be applied to genomic data from three island species of Drosophila: D sechellia, D. mauritiana and D. santomea which have split from their mainland ancestors relatively recently (250-500,000 years ago) and can be seen as independent replicates of speciation in very similar geographic and ecological settings. These species are unique because lab studies have revealed much about the genetic basis of a large range of traits involved in reproductive isolation, including genes that cause hybrids to be infertile and those underlying more complicated traits such as mating behaviour. However, their actual history of divergence is poorly known because current inference methods are limited to small datasets. In particular, we do not know how important gene flow during or after divergence has been. The new statistical method will allow me to compare the history of speciation in these three model systems in a number of ways. Firstly, I will ask whether species on islands closer to the mainland have experienced more genetic exchange with their mainland relatives than those further away. Secondly, I will test if divergence differs between different regions of the genome as predicted by current models of speciation and whether these differences are species-specific or universal. Finally, I will investigate whether genes known to be responsible for reproductive isolation can be distinguished against the genomic background by their different patterns of divergence alone. This would make it possible to identify such genes in other organisms where functional knowledge is not available through simple genomic scans.
People |
ORCID iD |
Konrad Lohse (Principal Investigator) |
Publications
Bunnefeld L
(2015)
Inferring Bottlenecks from Genome-Wide Samples of Short Sequence Blocks.
in Genetics
Hearn J
(2014)
Likelihood-based inference of population history from low-coverage de novo genome assemblies.
in Molecular ecology
Hickerson MJ
(2014)
Recommendations for using msBayes to incorporate uncertainty in selecting an abc model prior: a response to oaks et Al.
in Evolution; international journal of organic evolution
Lohse K
(2014)
Neandertal admixture in Eurasia confirmed by maximum-likelihood analysis of three genomes.
in Genetics
Lohse K
(2016)
Efficient Strategies for Calculating Blockwise Likelihoods Under the Coalescent
in Genetics
Lohse K
(2015)
Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation.
in Evolution; international journal of organic evolution
Smith G
(2012)
Model-based comparisons of phylogeographic scenarios resolve the intraspecific divergence of cactophilic Drosophila mojavensis.
in Molecular ecology
Stone GN
(2012)
Reconstructing community assembly in time and space reveals enemy escape in a Western Palearctic insect community.
in Current biology : CB
Description | I have: 1) Developed a new and general statistical framework to extract detailed information about the history of species and populations from genome sequence data. 2) Used this new method to make more detailed inference about the history of human populations, in particular when and where geneflow with Neandertals occurred. 3) Reconstructed the speciation process in a fruit fly model system. This research showed that species divergence can be triggered by large chromosomal rearrangements as predicted by theoretical models of speciation. 4) Ongoing and future work is comparing speciation histories across species to understand why some groups of organisms speciate more often than others. |
Exploitation Route | The new inference method has wide applicability beyond the context of speciation. For example, our inferences about past, natural hybridisation between wild boar and the endangered Visayan Warty pig will inform conservation/breeding programs for this species. More generally, understanding of the effects of demography on genetic diversity is vital when screening genomic data for signatures of past selection. |
Sectors | Agriculture, Food and Drink,Environment |
URL | http://planetearth.nerc.ac.uk/news/story.aspx?id=1654&cookieConsent=A |
Description | Our research on human/neandertal divergence and introgression has captivated the imagination of the general public and has raised awareness about the fact that genetic data contain detailed information about the recent history of populations. |
First Year Of Impact | 2014 |
Impact Types | Societal |
Description | LEADERS award |
Amount | £18,746 (GBP) |
Organisation | Scottish Universities Life Sciences Alliance |
Sector | Academic/University |
Country | United Kingdom |
Start | 08/2013 |
End | 02/2015 |
Description | Demographic inference of South East Asian Sus species |
Organisation | Wageningen University & Research |
Country | Netherlands |
Sector | Academic/University |
PI Contribution | I have developed an analytical approach for fitting histories of population divergence and introgression/hybridisation from genome sequences. |
Collaborator Contribution | Martien Groenen's group has applied this method to mammalian genomes, including humans, Neandertals and pigs. In patricular, we estimated the timing and amount of introgresion/hybridisation between wild boar (Sus scrofa) and the Visayan Warty pig (Sus verrucosus), an endangered species in Island South East Asia. |
Impact | doi/10.1111/mec.12958/abstract doi: 10.1534/genetics.114.162396 |
Start Year | 2012 |
Description | Radio interview BBC Radio Scotland |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Public/other audiences |
Results and Impact | I was approached by several media outlets, members of the public and a colleague at Edinburgh University working on Neandertal remains. Further media attention. |
Year(s) Of Engagement Activity | 2014 |
Description | UoEdinburgh Press Release |
Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Media (as a channel to the public) |
Results and Impact | Our research on Neandertal human divergence and introgression was covered widely by national and international media outlets and blogs including: BBC Radio Scotland, Daily Mail, Evenening Telegraph, Herald, The Border Mail (Australia), Dutch TV, NERC Planet Earth. Judging from online comments, the this media coverage generated a lot of discussion about human evolution/ancestry in the general public. |
Year(s) Of Engagement Activity | 2014 |
URL | http://planetearth.nerc.ac.uk/news/story.aspx?id=1654 |