Interview with the author: Killer whale genomes reveal a complex history of recurrent admixture and vicariance

By Robert Pittman – NOAA (http://www.afsc.noaa.gov/Quarterly/amj2005/divrptsNMML3.htm%5D), Public Domain, https://commons.wikimedia.org/w/index.php?curid=1433661. Two killer whales jump above the sea surface, showing their black, white and grey colouration. The closer whale is upright and viewed from the side, while the other whale is arching backward to display its underside.

In this study, Foote et al. study the complex demographic history of killer whales and show how episodic gene flow is ubiquitous in their natural populations. This observation adds to the incresing recognition that the traditional geographical characterization of populations (i.e., allopatry, parapatry, and sympatry) is dynamic over time. Although in general it is difficult to perform deep sampling across the range of a species, cut through artificial taxonomic boundaries, and access enough genomic resources for a taxon, their journey is a great example as to how to do this, and how powerful population genetic methods can reveal the history of vagile and amply distributed species on earth.

What led to your interest in this topic / what was the motivation for this study? 
I’ve been working together with Phil Morin at Southwest Fisheries Science Centre for the last ten years, using genetic data to try and unravel the complex demographic and evolutionary history of killer whales. Some of the key questions have been, whether killer whale ecotypes arose from independent founder events and secondary contact, or through gradual divergence in sympatry. This study started out trying to model those processes (in collaboration with Laurent Excoffier) using genomes we had previously sequenced for a subset of the well-described killer whale ecotypes. We struggled to find a good model to fit the data, and it eventually became clear that we just had too few pieces of the jigsaw to be able to see the complete picture. We decided to cast a wider net and looked back at our previous global study published in Molecular Ecology in 2015, to select a dataset of samples that was representative of the global genetic variation in killer whales for genome sequencing. Having worked in the Centre for GeoGenetics, Copenhagen and the CMPG, Bern – both largely focused on human genetic variation, and being keen follower of that literature, it was a great opportunity to apply methods developed in that field on the killer whales.

What difficulties did you run into along the way? 
Arguably, the biggest hurdle to overcome was bringing clarity to the very complex relationships between these killer whale populations. This was exacerbated by trying to include too many analyses in earlier drafts. We had a draft manuscript ready almost a year ago, which consisted of two parts: the demographic and evolutionary history of these populations; and the genomic consequences of these different demographic histories. However, this manuscript had become a behemoth! Thankfully, Jochen Wolf, one of the first coauthors to tackle a full read-through of this weighty tome, suggested this might be better digested in separate sittings. So the paper became focused on the evolutionary history and hopefully is an easier read…thanks to Jochen.

What is the biggest or most surprising finding from this study? 
The ghost ancestry in the Antarctic types, which was something I had suspected we might find, was only really possible to test for due to methods being released as we were writing up the paper. Clearly, we weren’t the only ones thinking along these lines, as several other studies on species including seabass and bonobos released similar findings of ghost ancestry around the same time – this is really nicely highlighted in the perspective by Jacobs and Therkildsen, in the same issue of Molecular Ecology.

Moving forward, what are the next steps for this research?
A key interest is how variation in the genomic architecture, principally local recombination rate, influences the frequency of different ancestry components within a population and how that relates to past demographic history. As eluded to above, we have results on the impacts of these complex demographic histories in a study we are just finishing up. As a follow up, we will explore further the history of the ghost ancestry, to find out if it conveys any benefits (adaptive variants) or costs (mutation load), such as we see in Neanderthal ancestry in modern humans.  And ultimately we hope to better understand the underlying processes determining the genetic differentiation between sympatric killer whale ecotypes.

What would your message be for students about to start their first research projects in this topic?
I’d recommend having a good understanding of the concepts, methods and models commonly used in population genetics. I’ve been reading Matt Hahn’s Molecular Population Genetics book and Graham Coop’s Population Genetic Notes, which is freely available to download from Graham’s brilliant blog – gcbias.org. Often methods will give seemingly contradictory results, and so it is important to be able to understand how those analyses work to be able to puzzle out the different signals from different methods. The two resources above will also help you design your sampling scheme and plan your study out ahead of time, so that it is best suited to the question you are trying to address.  

What have you learned about science over the course of this project?
I feel I’ve learned a lot. It has been a labour of love, the sequencing even being partly funded by my Swiss pension scheme which I cashed in when I left Bern. So, I didn’t feel like I had to please anyone but myself, and to be honest, I thought it was such a complex story and quite species-focused that it wouldn’t be of broad interest. But in fact, it is the paper that I’ve had the most direct and positive feedback on from colleagues. So that has been both surprising and satisfying. The lesson I take from that is to always try and work on something that you are passionate about.

I also feel that as I was learning to better understand the methods and the analyses, I was trying to really hard to pass that on to the reader, assuming they may be as naïve as I was before I delved into this study. And based on the feedback, that is something that folk appreciate, and which makes the paper more intuitive and transparent. I have tried to expand upon this in a youtube video.

image
(a) Sampling locations of the individuals for which 26, 5× coverage genomes were generated (global data set). Marker colours are as per the PCA legend. An additional 20 low coverage genomes (ecotype data set) were used in some analyses, see Foote et al. (2016) for sampling locations. (b) PCA plots of the combined global and ecotype data sets, and (c) the global data set (one sample per population). (d) Individual admixture proportions, conditional on the number of genetic clusters (K = 2 and K = 3), for the combined global and ecotype data sets, and for (K = 2) (e) when only one 5× coverage genome per population from the global data set is included

Describe the significance of this research for the general scientific community in one sentence.
Genomes sequences are a record of the many genealogies that comprise our ancestry. Our study highlights how a relatively small number of genomes can reveal the complex relationship among populations, past and present, across the globe.

Describe the significance of this research for your scientific community in one sentence.
Our study highlights that marine scientists need to consider connectivity through time, to past populations, as well as space to better understand the genetic composition of present-day populations.

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out /  Change )

Google photo

You are commenting using your Google account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s