Guest post by Andrew Hendry: "Pitchfork Science: Guppies, Stickleback, and Darwin’s Finches"

The following post is an invited personal guest post by Andrew Hendry at McGill University, who kindly invited me to write a guest post on "Eco-Evo-Evo-Eco"/Erik Svensson

By Andrew Hendry

I study Trinidadian guppies, threespine stickleback, and Darwin’s finches, surely 3 of the top 10 canonical vertebrate evolutionary biology “model” systems. I thus fall at one extreme (or is it three extremes?) on the “pick a model system and use it to answer my question” versus “develop a brand new system all my own” continuum. Many students and postdocs find themselves facing their own decisions about where to position themselves along this continuum. Should they take the shortcut of working with an established system so they don’t have to work out the simple details and can get right to addressing the big general questions? Or should they forge their own path and become an expert in something brand new? It might seem, based on the above listing, that I consciously took the first approach but the reality is something quite different. In truth, I used a “follow your nose” coincidence-and-serendipity approach to study system choice. I here trace my own personal history in these research areas before closing with some general thoughts on how to choose a study system.

Why I study salmon - a 16 year old me with a steelhead from our cabin (Kispiox River, BC, Canada).

I worked on salmon for my MSc and PhD, largely because I grew up with salmon fishing as my primary passion. Thus, I began studying salmon simply because I liked them and liked fishing for them. This led me to choose an institution (University of Washington - UW), department (School of Fisheries), and supervisor (Tom Quinn) who were ideally suited to immerse myself in salmon work. As my graduate work progressed, I very gradually became more and more interested in general questions in ecology, largely through exposure to the research of other people in the department. I even started subscribing to Ecology in addition to – of course – Fisheries. Yet my thinking remained salmon-centric: “what can ecology tell me about salmon”. Nothing wrong with that, of course. Then, when visiting home for Christmas in 1994, I received from my mother a book: “The Beak of the Finch” by Jonathan Weiner. When your Mom gives you a book for Christmas and you then spend the next week at home… well, you better read it.

The laboratory for my PhD - Lake Nerka, Wood River, Alaska.

The book was amazing. It described in wonderfully readable prose the research of Peter and Rosemary Grant on Darwin’s finches in the Galapagos Islands. What struck me the most, while reading beside the heater vent looking out at the blowing snow and -40 C weather (literally!), was Jonathan’s description of how the Grants had documented generation-by-generation rapid evolution of finch beaks in response to natural selection resulting from environmental change. Wow – you can actually study evolution in real time! It was my own eureka moment and, in short order, I became captivated by the idea. As soon as I got back to UW after Christmas, I went to the library and photocopied EVERY paper on Darwin’s finches (ah, libraries and photocopying – the good [and bad] old days). From then on, almost as though my brain had achieved an alternative stable state, my thinking was inverted to become “What can salmon tell me about evolution.” 

My MSc and PhD work focused on sockeye salmon - this one in Knutson Bay, Lake Iliamna, Alaska.

Salmon did tell me a lot about evolution. I even edited a book (Evolution Illuminated, with one of my evolutionary idols, Steve Stearns) about merging evolutionary theory and salmon research. However, when one starts focusing on a topic (evolution) rather than an organism (salmon), one starts to become irked by aspects of the organisms that are not optimal for addressing the topic. Most notably, it is very hard to do experiments with salmon unless you have lots of water, lots of space, and lots of time. So, when thinking about a postdoc, I started talking to folks about which systems might allow me to better address basic evolutionary questions. I ended up moving in two directions.

The laboratory for my first postdoc. For more than a month of glorious weather, I camped on a small island in a small lake (Mackie Lake) at the end of a 4-wheel drive road. Those are my mesocosms floating in the lake and projecting from the island.

The first was the University of British Columbia (UBC) – because I didn’t want to go too far from my girlfriend (now wife) who was still at UW. I visited UBC and went from prof to prof telling them of my interest in a basic evolutionary question – the balance between divergent selection and gene flow – and asking if they knew of a system that would be good for testing my ideas. Many great suggestions were made, but Rick Taylor insisted he had the perfect system: Misty lake-stream stickleback – and he was right. So I started working on stickleback not because they were a model system, but because someone suggested they would be well-suited for my question and because it let me stay reasonably near my sweetheart.

A threespine stickleback guarding his nest.

The second direction came about through a conversation with Ian Fleming, who suggested that I should work with David Reznick on guppies. I hadn’t even considered this possibility, but I knew a bit about the system (it is also described in The Beak of the Finch) and it seemed cool. So I went to UCR and met with David and talked about how we might use guppies to study the interaction between selection and gene flow. David said he would be happy to help me with this work but that he didn’t have any money for me – and so I offered to write a full NSF proposal. I was just gearing up to do so when I heard that I had received an NSERC (Canada) postdoctoral fellowship to work with Rick Taylor on the Misty system – so off I went to stickleback, leaving guppies behind.

My favorite wild guppies captured in my first year of sampling, 2002.

UBC was great, an outstanding place for nurturing interest and insight into general questions in evolutionary biology, but one must eventually move on. My next postdoc was the Darwin Fellowship (I applied because of the title) at the University of Massachusetts (UMASS) Amherst, working with BenLetcher on salmon again (hard to shake the habitat). While at UMASS, my guilt started building about telling David I would write an NSF grant and then not having done so, so I went ahead and wrote one, which got funded on the second shot (after bringing in my salmony lab-mate from Tom’s lab, Mike Kinnison). So my work on guppies eventually developed owing to guilt about not carrying through on something I said I would do.

The laboratory for our guppy work - here the Paria River, Trinidad

While at UMASS, my office happened to be near that of JeffPodos, who was working on Darwin’s finches. Near the end of my Darwin Fellowship, Jeff received an NSF Career grant and had money to burn – I mean invest. Jeff knew of my interests and asked if I wanted to come along to the Galapagos on the project (he recalls me asking – or perhaps begging – to come with him), and of course I immediately said yes. So my work on finches was simply a case of being in the right place at the right time. It was every bit as exciting as promised that cold winter back in 1994. Several years later, Jonathan Weiner called to talk about my salmon work and I was able to tell him how influential his book had been and how it actually brought me (without any plan) to work on finches.

In short, a large amount of coincidence and serendipity determined my choice of study systems. Once in each of the three systems, I became enamored with them and never left. I have now 25 papers on stickleback, 22 papers on guppies, and 11 papers on finches, and I have no intention of ever pulling back from any of these systems. I have also published 33 papers on salmon, and I continually look for new opportunities for additional work on them.

The laboratory for our finch work, presided over by a marine iguana.

Peter Grant once told me that, in conversation with Daniel Pauly at UBC, Dan told him that he (Peter) was a “point person” whereas he (Daniel) was a “line person”: a point person being someone who takes a single subject/system (finches) and looks at every aspect of their ecology and evolution, and a line person being some who takes a single subject (fisheries) and looks at it across many systems. I guess that makes me a pitch-fork person – trying to go into depth in three systems. Of course, this means that I can’t get too deep in any one system, much to my frustration. However, comparing and contrasting results from the three systems has proven fascinating. For instance, I study ecological speciation in all three systems with essentially the same methods (catching, banding/marking, measuring, recapturing, genotyping) focused on revealing the same processes (disruptive/divergent selection, adaptive divergence, assortative mating, gene flow). The similarities and differences in results obtained from the three systems has proved very instructive and motivational. In fact, my favorite research talk involves walking through a comparative story of ecological speciation in the three systems.

Perhaps my favorite finch photo.

Beyond how many systems one works in, I need to return to the question of working with model (developed) versus new (undeveloped) systems. As noted earlier, a benefit of working in a model system is that one doesn’t have to do as much background work (although every system is nowhere near as well-understood as the impression given by the literature), whereas a cost is that you are never known as the expert in that system (because the experts are the senior folks working on the same thing). The cost-benefit payoff is not easy to calculate and so the temptation for many students and postdocs is to spend a lot of time debating the pros and cons of the different approaches. I think all this angst is a mistake (or at least suboptimal) and that one should instead follow one’s nose (and Mom’s book recommendations). I think everyone should work on the systems and with the people that they find the most interesting and inspiring – not the systems that have the best-described genomes (as an example). These inspiring systems might be model systems or they might be new systems or both (I also have students work on non-model systems), but they are – most importantly – the systems that feel right at the time, not the systems that have been rationalized based on a logical calculation of optimal career advancement. It worked out fine for me (and many others) – although I am sure my colleagues would argue I could still use considerably more career advancement.

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Resources:

An interesting perspective by Joe Travis on question-based versus system-based science: Is it what we know or who we know? Choice of organism and robustness of inference in ecology and evolutionary biology

Thoughts and reflections about the nature of selection from a NESCent-meeting in North Carolina

Posted by Erik Svensson

I just returned from a three-day working group meeting at "National Evolutionary Synthesis Centre" (NESCent) in Durham (North Carolina). The working group's topic is "Environmental and demographic determinants of natural selection", and there were 18 participants from the Australia, Canada, Sweden, the US and UK, i. e. a very multantional and scientifically diverse crowd, some of which you see on the pictures above and who you might recognize already. The organizers of this working group are Andrew MacColl, Adam Siepielski, Stephanie Carlson and Tim Coulson, four colleagues whose work I did know very well since before, but this was actually the first time we met IRL.

This working group will perform a meta-analysis and litterature synthesis on a favourite topic of mine: the ecological causes of natural and sexual selection on phenotypic traits in natural populations. I have been interested in this topic since my postdoc, especially the role of density-dependent natural selection on egg size, but also in later years when Tom Gosden and I studied spatial variation in sexual selection and its ecological consequences in the damselfly Ischnura elegans. 

 In spite of several decades of excellent selection studies in natural populations (summarized in a large meta-analysis ten years ago by Joel Kingsolver and colleagues), our knowledge about ecological agents (predators? competitors? parasites? climate?) are still very limited and far from quantitative. This is unfortunate, as natural selection is an ecological process, that might (or might not!) lead to evolutionary change. In fact, and to cite the great population geneticist Ronald Fisher in the famous opening sentence of his landmark volume The Genetical Theory of Natural Selection (published in 1930): "Natural selection is not evolution". Natural selection might lead to evolution - if the traits under selection are heritable and some other conditions are met - but need not to do so, and frequently does not.

Natural selection can for instance also reduce population size and cause extinction - and how often this is the case in nature we do not know. Nor is all evolutionary change due to natural selection - only extreme adaptationists would claim this. Much of evolutionary change can be due to - for instance - genetic drift, gene flow, recombination or simply neutral changes (for non-coding DNA). Thus, evolution and natural selection should not be confused - and one should not forget that one can study natural selection without any knowledge about genetics or the underlying genetic basis of traits under selection (Darwin is a good example of an evolutionist who knew more about natural selection than many molecular geneticists do today).

In this working group, we will search the litterature and add to already existing databases information about selective agents to those published studies where selection on phenotypic traits have been quantified already. Questions that can then be adressed include: How much of the variation in selection gradients can be explained by various environmental factors? What is the role of climatic factors and other abiotic factors vs. biotic factors like predation, competition, food supply or parasites? Do abiotic factors like climate and biotic factors interact - and could they even reinforce each other? We take up the challenge put forward by Michael Wade and Susan Kalisz in their important conceptual paper "The causes of natural selection" from 1990.

The questions are endless - and we know very little about the answers, but they are likely to be important. It is interesting that there is so much to do in this field and in the study of the ecology of selection in the "postgenomic" era, when we realize that the molecular revolution did not, and will not, solve all problems in evolutionary biology, and certainly not these ecological questions about the nature of selection on quantitative traits (whose genetic background is often due to many loci of small effects, resulting in the "missing heritability" problem).

The radical conclusion remains however: we do not need to know anything about neither quantative genetics or molecular genetics to study the ecological causes of selection - as this a question at an entirely different level of organization and  the ecological process of selection does not have anything to do with genetics, as so elegantly clarified and formalized by Lande and Arnold in their classical 1983-paper.

I am happy to have the opportunity to participate in a working group like this, and also impressed by a facility as NESCent - where synthetic work of this kind is funded - to the benefit of not only US scientists but also scientists from other countries. Hopefully, this working group will find some interesting new patterns and move the field forward - and perhaps help us to improve the empirical study of selection. I have already learned a lot - and hope to learn even more in the future. And that, after all, is the goal of science, not only publishing papers - which is of course also nice - but which is only one way of many others to communicate science. This blog post has hopefully also inspired and informed somewhat in that respect.

Scientific misconceptions, publication stress and criticism of molecular ecology as a research field

Posted by Erik Svensson

At Juha Merilä's research group blog, EGRU-blog, one often finds very interesting and provocative posts, that stimulates self-reflection and critical thinking. Here is one such post, which raises some critical questions about the field of molecular ecology and the lack of rigour among some of the scientists defining themselves as belonging to this novel field.

This short post actually refers to a recent Invited Review, which is likely to upset some molecular ecologists, as it is very provocative and questions much of the research practices in this very young and technologically-oriented discipline. I do not necessarily endorse everything in this article, and some points that are discussed are beyond my expertise and research interests. As for myself, I do not get very upset or feel very threatened by the message, because I am not a molecular ecologist (and will never become one), even though we have used molecular techniques in our research lab for several years now, and published several papers in the journal Molecular Ecology as well (e. g. this, this and this).

But using molecular techniques, like we have done in these studies, and even endorsing them, is not the same thing as being a molecular ecologist, in my opinion. It is not even enough to publish in the journal Molecular Ecology, I think. I, for myself,  would never define myself as molecular ecologist. Rather, I define myself as an old-fashioned evolutionary biologist interested in the ecological aspects of evolutionary change. Or sometimes I simply define myself an evolutionary ecologist, who is prepared to use observations, field and lab experiments, quantitative genetics and molecular techniques, depending on what is needed and what question that is being adressed.

In contrast, molecular ecology as a field, as I perceive it, is a primarily a discipline defined by techniques and the use of molecular markers, rather than being defined by research questions. And that is why I have never been very interested in this field, as I tend to be more interested in conceptual problems in ecology and evolution, while not being hostile towards new techniques, when they help to solve these classical problems (which is not always the case, however). Molecular Ecology partly grew out from behavioural ecology during the eighties and nineties, as new molecular methods for determining paternity in birds and other animals were developed (first DNA-fingerprinting and later microsattelites). Later, the field came to include many other research questions being adressed by the use of molecular markers, such as phylogeography and molecular population genetic structure etc.

The current review is - interestingly - published in Molecular Ecology - which I think is to the benefit of this outlet as it shows some self-criticism of the same field that the journal is built upon. Hopefully, this article will help to promote self-reflection and critical thinking, both among molecular ecologists (the main target), but also other biologists using molecular techniques. The paper is Open Acess and can be downloaded here. 

 Here are some excerpts, and quite critical and provocative quotations from the paper (Abstract and full reference given below this post):

"Many misconceptions in the various subdisciplines of molecular ecology arise as a consequence of the huge amount of data that can be relatively easily and rapidly generated and analysed. There are many more automated DNA sequencers than classes in population genetic theory, and as self-educated molecular ecologists contribute in professional service, we sometimes see misconceptions perpetuated by journal authors, reviewers and editors."

And:

"At the end of this review, many readers will still believe that if they can properly format data for mega (Tamura et al. 2011) or arlequin(Excoffier et al. 2005), they do not need population genetic theory, they can pick it up along the way, or all the information they need is in the manual. Considering the high error rate (49.9%) in publications of a simple calculation of a population genetic parameter revealed bySchenekar & Weiss (2011), our answer is this: about half of you are right."


Finally, here is some very harsh criticism against the data publication culture in the field of molecular ecology,  and the tendency to crank out too many papers, with too many authors and ignoring much of the classic work that has already been published and which would be relevant to cite:

"As a result of these technological advances, not just in DNA sequencing, but also in computing power and web-based manuscript review, the trend has been for more data per publication, shorter time to publication and more publications per author in the field of molecular ecology. For example, 181 recently hired tenure-track faculty world-wide had an average of 2.9 years of postdoctoral experience and an average of 11.75 (maximum 45) peer-reviewed publications at the time of hire (Marshall et al. 2009). By comparison, a search of Web of Knowledge (Thomson Reuters formerly ISI) most highly cited authors returned 12 that completed their doctoral dissertations before 1990 and whose CVs are available online. These researchers produced an average of only 4.6 ± 0.2 publications by three years after graduation. Likewise, a dissertation in one of the disciplines of molecular ecology prior to 1990 was typically based on sequences from a single-locus and samples sizes of tens of individuals, whereas today dissertations are routinely expected to include several hundred lengthy sequences for multiple genes.

This increased expectation and rate of publication also results in ever more submissions to journals, which increase rejection rates due to space limitations, and that builds pressure on authors to claim the first, biggest or best study for submissions to high-impact factor journals. Claiming to be the first study to ever show some result is facilitated by an eroding knowledge of the classic literature."

STEPHEN A. KARL1, R. J. TOONEN1, W. S. GRANT2, B. W. BOWEN1

Article first published online: 11 MAY 2012DOI: 10.1111/j.1365-294X.2012.05576.x 

Abstract: The field of molecular ecology has burgeoned into a large discipline spurred on by technical innovations that facilitate the rapid acquisition of large amounts of genotypic data, by the continuing development of theory to interpret results, and by the availability of computer programs to analyse data sets. As the discipline grows, however, misconceptions have become enshrined in the literature and are perpetuated by routine citations to other articles in molecular ecology. These misconceptions hamper a better understanding of the processes that influence genetic variation in natural populations and sometimes lead to erroneous conclusions. Here, we consider eight misconceptions commonly appearing in the literature: (i) some molecular markers are inherently better than other markers; (ii) mtDNA produces higher FST values than nDNA; (iii) estimated population coalescences are real; (iv) more data are always better; (v) one needs to do a Bayesian analysis; (vi) selective sweeps influence mtDNA data; (vii) equilibrium conditions are critical for estimating population parameters; and (viii) having better technology makes us smarter than our predecessors. This is clearly not an exhaustive list and many others can be added. It is, however, sufficient to illustrate why we all need to be more critical of our own understanding of molecular ecology and to be suspicious of self-evident truths.

Minisymposium May 24 2012: "Biogeography and Evolution"

We are happy to announce an exciting Minisymposium entitled "Biogeography and Evolution" on May 24 2012 that will take place on the afternoon the day preceeding Anna Runemarks PhD-thesis defence (May 25). We have four excellent speakers that will present some exciting talks this afternoon. This symposium is open for everyone, whether from the Biology Department of from elsewhere. Full details of the programme and the titles of the talks are presented below:

Minisymposium on Biogeography and 

Evolution

                 

May 24, 13.00 - 16.00                               

"Blue Hall", Ecology Building, Department of Biology, Lund

13.00-13.40 Scott V. Edwards (Harvard University, USA)  “The phylogeography-phylogenetics continuum: a look to the future”

13.50-14.20 Jessica Ware (Rutgers University, USA) "Here be dragons: biodgeography and age of Petaluridae, the petaltail dragonflies"

14.30-14.50 Coffee

14.50 - 15.20 Alexandre Antonelli (Gothenburg University, Sweden) "Ecology meets Biogeography: A Multi-Disciplinary Approach to Study Neotropical Diversification"

15.30- 15.50 Folmer Bokma (Umeå University, Sweden) ”Why species may not adapt”

15.50 - 16.00 Discussion and concluding remarks

Symposium open for all interested. No registration required.

Welcome!


Bengt Hansson, Anna Runemark & Erik Svensson

Lab-meeting on the evolution of plasticity in changing environments

This Wednesday (January 11 2012), we will discuss a relatively recent theoretical and conceptual paper in PLoS Biology entitled "Adaptation, plasticity and extinction in a changing environment: towards a predictive theory".  You can download it here.


Although this paper was published as recently as in 2010, but has already received 79 citations - a sign of a quite an influential paper. This is not surprising as it connects such topics as climate change, thermal adaptation and niche modelling with the evolution of phenotypic plasticity - all very important and central topics in ecology and evoutionary biology. Below you will find the Abstract for the paper. One of the co-authors is legendary evolutionary quantitative geneticist Russel Lande, by the way.

Time: Wednesday, January 11, 2012
Place: "Argumentet"

 

Summary 

Many species are experiencing sustained environmental change mainly due to human activities. The unusual rate and extent of anthropogenic alterations of the environment may exceed the capacity of developmental, genetic, and demographic mechanisms that populations have evolved to deal with environmental change. To begin to understand the limits to population persistence, we present a simple evolutionary model for the critical rate of environmental change beyond which a population must decline and go extinct. We use this model to highlight the major determinants of extinction risk in a changing environment, and identify research needs for improved predictions based on projected changes in environmental variables. Two key parameters relating the environment to population biology have not yet received sufficient attention. Phenotypic plasticity, the direct influence of environment on the development of individual phenotypes, is increasingly considered an important component of phenotypic change in the wild and should be incorporated in models of population persistence. Environmental sensitivity of selection, the change in the optimum phenotype with the environment, still crucially needs empirical assessment. We use environmental tolerance curves and other examples of ecological and evolutionary responses to climate change to illustrate how these mechanistic approaches can be developed for predictive purposes.

Lab-meeting on epigenetic inheritance and evolution

Following the suggestions of Machteld Verzijden and Anna Runemark, I suggest we denote next lab-meeting to discuss epigenetic inheritance and its (possible) evolutionary consequences to epigenetic inheritance. I suggest that we discuss two recent papers, one more theoretical in American Naturalist by Troy Day and Russel Bonduriansky which can be found here, and a review in Nature Reviews Genetics by Danchin et al. which can be found here. I post the Abstract of that paper below.

Please read both these papers, and not in the last minute, as it is a difficult topic, but the more we know in advance, the more enlightened will the discussion be.

Note that next lab-mating will take place in "Argumentet" between 10.00 and 12.00 on Tuesday 6 September 2011. After that, our regular lab-meetings will take place between 10.00 and 12.00 on Thursdays. Fika volunteers are always welcome.

Beyond DNA: integrating inclusive inheritance into an extended theory of evolution
Danchin, E (Danchin, Etienne)1; Charmantier, A (Charmantier, Anne)2; Champagne, FA (Champagne, Frances A.)3; Mesoudi, A (Mesoudi, Alex)4; Pujol, B (Pujol, Benoit)1; Blanchet, S (Blanchet, Simon)1,5
Nature Reviews Genetics 12: 475-486
Abstract: Many biologists are calling for an 'extended evolutionary synthesis' that would 'modernize the modern synthesis' of evolution. Biological information is typically considered as being transmitted across generations by the DNA sequence alone, but accumulating evidence indicates that both genetic and non-genetic inheritance, and the interactions between them, have important effects on evolutionary outcomes. We review the evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, and outline methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations. These issues have implications for diverse areas, from the question of missing heritability in human complex-trait genetics to the basis of major evolutionary transitions.