First EXEB-meeting in 2016: on speciation, ecological opportunity and latitude

                                



















Crab spider (Misumenia vatia) with prey. Photo: Erik Svensson

Posted by Erik Svensson 

"Evolution in Sweden 2016" is now over, and in my opinion it was a great success. You can see photos from this meeting here, and we can also briefly summarize our general reflections about this meeting on the first EXEB-meeting, which I post information about below. 

On this first EXEB-meeting of 2016, I want to discuss a recent paper published as a "Presidential Adress" in American Naturalist by Dolph Schluter, entitled "Speciation, ecological opportunity and latitude". 

I saw Dolph give a talk about this last year at a speciation-meeting in California, and I think that he is a very thoughtful scientist who has stimulated my thinking and influenced many other ecologists and evolutionary biologists. Hopefully, we will have a good discussion about this paper. But as usual, we will start the meeting with some general reflections, summary of impressions of "Evolution in Sweden 2016" and we can also hear a bit from Tobias and Nathalie's trip to Australia, as well as mine, Katie's and John's trip to Argentina. I might even bring some pictures to show. 

Time: Tuesday, January 19, at 10.00

Where: "Argumentet", 2nd floor, Ecology Building

Abstract: Evolutionary hypotheses to explain the greater numbers of species in the tropics than the temperate zone include greater age and area, higher temperature and metabolic rates, and greater ecological opportunity. These ideas make contrasting predictions about the relationship between speciation processes and latitude, which I elaborate and evaluate. Available data suggest that per capita speciation rates are currently highest in the temperate zone and that diversification rates (speciation minus extinction) are similar between latitudes. In contrast, clades whose oldest analyzed dates precede the Eocene thermal maximum, when the extent of the tropics was much greater than today, tend to show highest speciation and diversification rates in the tropics. These findings are consistent with age and area, which is alone among hypotheses in predicting a time trend. Higher recent speciation rates in the temperate zone than the tropics suggest an additional response to high ecological opportunity associated with low species diversity. These broad patterns are compelling but provide limited insights into underlying mechanisms, arguing that studies of speciation processes along the latitudinal gradient will be vital. Using threespine stickleback in depauperate northern lakes as an example, I show how high ecological opportunity can lead to rapid speciation. The results support a role for ecological opportunity in speciation, but its importance in the evolution of the latitudinal gradient remains uncertain. I conclude that per capita evolutionary rates are no longer higher in the tropics than the temperate zone. Nevertheless, the vast numbers of species that have already accumulated in the tropics ensure that total rate of species production remains highest there. Thus, tropical evolutionary momentum helps to perpetuate the steep latitudinal biodiversity gradient.

On powers and pitfalls of "Next-generation sequencing" in ecology and evolutionary biology

These days there is a lot of buzz about so-called "Next-generation sequencing" techniques, i. e. the novel molecular methods that allows ecologists and evoutionary biologists to rapidly sequence the entire genomes of their favourite organisms. A lot is promised by enthusiastic proponents, and it is understandable and easy to get carried away and to think that all interesting problems will be solved in the near future. As usual, when it comes to new techniques and fashionable scentific "bandwagons, it is healthy with some sound scepticism and critical attitude. I found an excellent such criticial perspective on the interesting and thoughtful blog "The Molecular Ecologist", which is worth reading. Here are som excerpts, but you should read it in full:


“Developing genomics tools for ecological organisms is desirable because we can study a wider range of phenotypic traits over evolutionary timescales and in more populations than was possible previously. Through this we are likely to gain a more realistic and comparative understanding of how selection works on natural levels of genetic variation, where this genetic variation comes from and how it is maintained.” Stapley et al. 2010 (TREE)

Okay let’s just get this out of the way. We’re way past calling next generation sequencing technologies, “Next Gen.” I mean, really isn’t Next Gen, yesterday’s news? With the advent of the third generation sequencing technologies that can sequence a single-molecule of DNA, we’re out of date in our terms.

The blogger criticizes the often made rather arrogant arguments that next-generation sequencing will solve many of the "mysteries" about the genetics of adaptation that was not possible to study before, while in reality, many workers in the classical model systems knew a lot since before:


In this article, Stapley et al. (2010), suggest that ecologists tend to have a good idea of what traits might be involved in adaptation for their study organism. They also suggest that geneticists know a lot about the genomic architecture of a few classical model organisms but very little about the ecological relevance. This argument is a little bit of a strawman, because it sets up a false opposition between ecology and genetics. In their eyes, the importance of this technology is that it will make it easier to integrate both ecological and genomic data and to develop for ecologically interesting organisms “a range of genomic resources such as whole genome sequences, transcriptome sequences, and genome-wide marker panels can be generated within the scope of a three-year grant.”

When I first read this statement, I thought that the authors had found a practical way to explain the rate at which genomic data can be generated. But then I realized how uncomfortable the phrase, “can be generated within the scope of a three-year grant” made me feel. And while I can’t put my finger on the exact reasons, I think it’s because it underscores the stark reality that research has to operate within the confines of short-term constraints. Clearly the authors mean that this will shorten the timeframe for researchers to start answering the interesting questions on any organism.

Moreover, using next-generation sequencing techniques on "any" randomly chosen organism is unlikely to generate any interesting data per se, if we know little about the ecology and natural history of the organism in question. It will only be interesting if it already is a well-characterized "model organism", in the sense that it has been extensively studied (preferably experimentally and in the field) for many years, and preferably decades. Interesting "questions" do not pop out of the blue and by themselves, but they are only relevant if there is good natural history knowledge about the organism in question. In other words, if you do not have a past research experience of your creature for many years and know "what to do", it will hardly be worth the money and effort to do next-generation sequencing, because you will be flooded with useless genomic information that you will not know what to do with:



However, the link between generating genomic data for interesting ecological organisms and how high-throughput sequencing technology has already reinvigorated current studies of the genetic basis of adaptation is missing something. The tacit implication is that because we can use HTST to create extensive genomic toolkits on non-model organisms, we should be able to gain a stronger understanding of how selection operates on ecologically relevant variation. And thus answer some of the questions that have “puzzled ecological geneticists for decades.”

I don’t disagree that we’ll move science along, but all of the non-model organisms described in the review have had extensive conceptual legwork contributed by many, many scientists over several years. It is because these biological systems are so highly developed conceptually that the power of HTST can be fully realized. 

For example in the three-spine stickleback system, it has taken several generations of grad students and postdocs to work out that replicate isolated freshwater stickleback populations were independently derived from their oceanic ancestors, that there is no gene flow between these isolated populations of freshwater habitats, that there is significant variation in behavior, life history, and morphology, that diversification happened very rapidly, and that selection has acted in parallel in these different isolated freshwater habitats evoking similar phenotypic trajectories at local, regional and global scales (the references are too numerous to cite so I’ve included a select few: Orti et al. 1994 Evolution, McKinnon and Rundle 2002 TREE, Hohenlohe et al. 2010 PLoS Genetics).

Lastly, and very importantly, next-generation sequencing techniques can be used in the study of parallell evolution and speciation, but it will not pick up all genes involved in adaptation if there are historical contingencies and if different genotypes contribute to the same phenotype. Here, we'll have to relly on other techniques, such as informed guesses and searching for candidate genes with a priori known function: 


In the case of the stickleback system, Baird et al. 2008 and subsequently, Hohenlohe et al. 2010 used Illumina-sequenced RAD tags to gather genome-scale sequence data on natural populations. The data confirmed previous work that freshwater populations were independently derived from the oceanic populations. Furthermore, using high-throughput sequencing technology (RAD-tags), researchers identified 9 genomic regions (3% of the genome) that were differentiated between the two ecotypes (freshwater and oceanic) and thus, putative candidate regions associated with adaptation to freshwater. Some of these genomic regions co-localized with previously identified loci of major effect (e.g. the Ectodysplasin A (Eda) locus). But using this HT sequence data, researchers found several additional regions showing parallel differentiation across independent populations. The power of this much data is that now there is a list of novel candidate regions that may be important in adaptation to freshwater.


Even more interesting is that the data generated from HT sequencing did not find elevated divergence in a region previously identified as underlying a major phenotypic change between the marine and freshwater fish. This pelvic structure, a bony stomach with spines, is present in the marine fish but reduced in the freshwater. The region responsible is a cis-acting tissue-specific enhancer located in the Pituitary homeobox transcription factor 1 gene (Pitx1) found at the telomeric end of linkage group seven (Chan et al. 2008 Science) . So why did high-throughput sequencing data, which provided 45,000 SNPs to the researchers not detect this locus? Hohenlohe et al. (2010) suggest that multiple alleles were selected in different freshwater populations leading to a soft sweep pattern. If, as Hohenlohe et al. suggest, that the soft sweep pattern is true, then using only high-throughput sequencing data to detect regions of adaptive significance could potentially lead to a bias against detecting this form of selection.

High-throughput sequencing technologies do allow each lab to cheaply and in a relatively quick timeframe generate a specific type of genomic data that can inform our understanding of how ecology impacts the genomic architecture of an organism. But it does not mean that within the scope of a three-year grant we will generate anything remotely resembling a detailed picture of the genetics of adaptation. This rich picture will be formed after several decades of hair-pulling by grad students, postdocs and their supervisors all of whom will toil away testing, challenging and advancing our understanding of adaptation.

So what should we conclude then? Next-generation sequencing is dead, long live phenomics", perhaps? Only time will tell. There is clearly a reaction and a movement away from the naive reductionist world-view created by genomics, and increasing awareness that the phenotype should be put back in to the centre of evolutionary biology. My educated guess is that this trend will continue and grow in the near future, as many are gathering messy and large data-sets from next-generation sequencing, and will struggle to get any meaningful results from these data. What we can conclude already now, I think, is that (as usual) new techniques promise more than they can deliver, and we will never find the "silver bullet" method that explains everything. As usual, it is the ecological and evolutionary questions that must be at the centre of attention of any investigation. A dose of healthy scepticism is, however, usually very helpful. And do not forget to read the classics and learn your natural history. That will help a lot, also in the future. 

Interesting blog about "Eco-evolutionary dynamics" by Andrew Hendry's lab

Those of you have met Andrew Hendry before, either in Vienna during the "Speciation"-meeting last week, or last year when he was the external opponent on the PhD-thesis by Fabrice Eroukhmanoff, might enjoy this blog from his research laboratory. His lab seem to have a similar attitude as ours when it comes to public outreach and using social media, which is nice. A general theme of their blog is "Eco-evolutionary dynamics", which fits well with the kind of research Hendry et al. have been pursuing in recent years, using sticklebacks, guppies and Galápagos finches as study organisms. Enjoy!

Adaptation driven by novel mutations or from selection on standing genetic variation?

Our collegue Hopi Hoekstra at Harvard University in the US, who visited us in August last year, has a paper in one of the last issues of Science. You can read a brief report on the website Science Daily here.

At first I was not very excited about this paper, as it appears to be the usual story about the melanocortin receptor (MC1R) and how it affects coat colour patterns in various mice populations, a story that by know is sufficiently wellknown and established so one wonders what remains to be discovered.

MC1R is responsible for dark coat colour in mice that occur in dark habitats (see above), e. g. on the dark lava flows in Arizona, that Hopi Hoekstra has previously studied together with her colleague Michael Nachmann.

However, this new paper has a new twist: it appears as if selection has acted on a novel mutant in deer mice in Nebraska, and this novel that apparently appeared in the population shortly after the last Ice Age, about 8 000 years ago.

Catherine Linnen and Hopi have analyzed genetic variation among these different mice populations and estimated the age of the allele that causes light coat colour in the mice. Light coloured mice carry a certain allele at a gene called Agouti, and this allele is quite young as it shows evidence of a selective sweep through reduction in DNA sequence diversity around that particular allele. Linnen and Hoekstra have thus used the well-known statistical approach of coalescense analysis to infer the age of the novel mutation at the Agouti locus that is causing light coat colour.

This result is important, as it provides some contrast to recent suggestions that novel mutations might not be that important in cases of rapid evolutionary change, which have instead emphasize selection on standing genetic variation in rapid evolutionary change. For instance, rapid evolutionary change need not always to rely on standing genetic variation as suggested by the findings from other systems like sticklebacks. The alternative is instead that rapid adaptive change is driven by a process by which selection in novel environments "picks up" and favours alleles that already segregated in the ancestral population, rather than "waiting" for the emergence of rare novel beneficial mutations (that might take long time to appear).

This process is sometimes also called phenotype sorting, referring to how a polymorphic and variable base populations might become transformed in to a new (monomorphic and less variable) population through the selective increase and selective loss of already existing phenotypes, which are then "filtered" by selection in the novel environment. Something along these lines appears to also be the case in the freshwater isopods that we have studied in our group, and we discussed this earlier this year in a paper published in Journal of Evolutionary Biology, which you can find here.

In summary, the relative importance of selection acting on novel mutations vs. standing genetic variation is probably something that will be discussed a lot the coming years in evolutionary biology and ecology.