Five years ago, I landed in Montréal for a PhD in the Faculty of Education, bringing with me my experience from the Greek rendition of environmental education. During my first term at McGill, I discovered that I was allowed to enroll in any graduate course (was this a glitch in the system?), so I registered to a graduate course taught by Andrew Hendry under the name Advanced Evolutionary Ecology. The course went well except from some awkward moments like the day when I took off my wet shoes in Andrew’s office during lecture time -- I was caught unprepared by the speed that winter had succeeded fall at the McGill downtown campus.
Nevertheless, those days were intellectually rewarding and full of new ideas. One day in that course, I sensed the scholarly need to expand the concept of the adaptive landscape in order to incorporate environmental change, and I thought that I have found a way to do that. Soon, I presented the idea to the class, got an A for the course, and Andrew encouraged me to work on the idea and gave me a couple of literature suggestions to explore. I didn’t really understand why did I need to keep reading, for all I knew it sounded like an interesting idea and once I laid it out, it would receive its criticism, and people could just decide whether it was useful or not. Nevertheless, I complied and did my homework. After a while, I returned to the professor and declared: I checked the literature, I’ve found nothing like it. The idea was apparently mine and we ought to spread the word. The sage professor responded with a couple of sibyllic words. He said something like: I don’t think that the idea is yours, but even if it was, people will take offence in you claiming that it was. In any case, he continued to encourage me to learn more on the topic and seek reviews from specialists on the field. Hence, I got some pleasing reviews from renowned Swedish professors, including Erik Svensson from Uppsala University who commented that “My initial attitude was not to expect much new, given that so much have already been written about this topic. However, what I found, after reading through the MS was a creative paper where the author has clearly worked hard to “think out of the box”, and has to – to some extent – been able to think along new lines.” He also suggested to revise the paper and rewrite it in a more ‘scientific’ way.
These were good news but the problem was I didn’t really know how to write a scientific paper since I wasn’t even a scientist. At that point, I asked from classmate and Andrew’s PhD student Victor Frankel to help me out. Luckily, he accepted and he did help me to rewrite the paper in a more scientific fashion. As we were ready to submit (already 3 ½ years after the initial draft) Victor decided to send our paper to Ben Haller asking for a review. Indeed, Ben studied the paper and sent it back to us with ample feedback: his comments were knowledgeable, specific, and poignant. I thought I had learned to appreciate hard criticism by then, but when I saw Ben’s comments on one of our diagrams, I thought that it went too far: “It is striking just how much this looks like one of the diagrams in Simpson 1944. I would say the conceptual model you’re presenting here goes back at least that far”, and “This doesn’t even feel like sufficient credit to him [Simpson], though, given his actual figure that I mentioned above, which is virtually identical to your 5b in all important details.” Now, that does it, I thought. I dropped anything else and went straight to the Schulich Library looking for the single copy of the 1944 Tempo and Mode in Evolution by George Gaylord Simpson trying to see what he was talking about. As I browsed the book in disbelief, I was sure that Ben (whom I had never met) recalled an irrelevant part of the book and was just trying to be mean. But it turned out that Ben was right. There it was: In a short passage accompanied by a diagram in the old book, Gaylord Simpson was proposing an environmental expansion of his ‘selection landscape’. The terminology in the book was very different than ours, the axes in the graph were inversely placed and the whole perspective was unlike ours, but the central idea was virtually the same. So, it turned out that our ‘new’ idea was outdated by 70 years, it was already proposed by one of the founders of the adaptive landscape. In the following moments, my thoughts went down a twisted path. Gaylord is long dead, I thought, his book isn’t on line, so maybe I could travel, find the few remaining copies at the world’s libraries, and tear out that single page. My instantaneous impulse was to destroy this fragment of knowledge that deprived me of the paternity of my idea. The idea was absurd, but this instantané helped me understand something about myself and how I was taken over by ambition, thinking that it wouldn’t do much harm to steal away a late man’s credit. A fault confessed is half redressed, as they say.
So, as it turned out, my original idea was not original at all. Interestingly enough, this revelation didn’t have a great impact on the paper itself. The paper was still publishable, yet we ought to give to Simpson more credit than we already did and explain that our paper was actually a revisit to his original ideas. It turns out that people rediscover ideas and methods all the time, and there is always room for updated renditions of old ideas. The bulk of intellectual progress comes from the translation, rendition, application, and interpretation of old ideas. However, that did not answer the question: Why on earth did no one return to this particular idea even though Simpson’s 1944 book was so widely read and referenced? The feedback we got for the eco-evolutionary expansion showed that there was an actual need for such a method. My explanation is that Simpson was way ahead of his time, trying to sow a seed in a field that did not exist back then. In 1944, an overlap or convergence between ecology and evolution was nowhere to be seen; ecology did not even exist as a field. Today, the niche between evo and eco is no longer an epistemological terra incognita. The science has progressed since then, and a few scholars are pioneering the synthesis between eco and evo. Exposed to the teaching and writings of these scholars, basically Andrew Hendry’s, we rediscovered the eco-phenotypic landscape in response to the need for a representation that brings ecology closer to evolution. In this process, nothing is really created ex nihilo. Our teachers were in turn influenced by their teachers, and carry on their set of ideas and problematics from generation to generation. However, save Ben and a few historians of science, we usually don’t read the old stuff all too carefully. We sometimes rely on secondary sources, or trust more modern renditions of the classic literature, because these are closer to the contemporary needs and scientific ethos. Yet, information is lost in this conveyor belt.
On a personal level, this has been a humbling experience. I now see the self indulgence in thinking I was able to produce original ideas. Not that it’s impossible to produce new ideas, especially when you are newcomer in a field. It’s just that, when a problem was standing out there for enough time, most probably someone else has solved it before you even knew. This is just because so many intelligent people have been thinking on the same problems, for such a long time. To cut it short, it’s hard to have new ideas in an old world. So, yes, it is imperative to scrutinize the literature before making any claims. It’s also a good idea to moderate any clams one decides to make. At the same time, these humbling realizations just meant that my education was working. Authentic education can’t be about inflating our egos. Conversely, the process of learning, of taking stock with the volume of knowledge accumulated over the ages, is meant to be a humbling experience. What drives us to this effort? According to Lonnie Aarssen, editor of Ideas in Ecology and Evolution, it’s an “attraction to delusions of being able to project an ‘extension of self’—a memetic legacy—into the indefinite future” (Aarssen 2017).
All these have also given me an idea about how science works. I do no longer believe that ideas can be owned. Instead, we are more like hosts for ideas, which seem to be having a life of their own jumping from mind to mind. Ideas are sometimes transmitted in dormant states, following their own life cycles, in many cases outliving us. Dawkins has effectively described this process in his memes metaphor. Following is a link for the paper itself, an extract from the paper discussing sympatric speciation and a part on heterosis that we took out of the final text because one of the reviewers found it problematic. We did not have the courage or time to rewrite the part on heterosis, but there might be some value in sharing it, as indicated by Ben Haller’s comments below. Many thanks to Ben for allowing us to share his feedback.
Figure 2. A qualitative representation of Bergman’s rule on the unconstrained adaptive landscape (individual fitness peaks shift under the influence of environmental change).
A mechanism for sympatric speciation
This section uses the eco-phenotypic landscape to describe a speciation model within a continuous population distribution. Numerous studies have noted gene flow as an obstacle to speciation (Kirkpatrick and Barton 1997, Rousset 2000, Hendry et al. 2009, Berner et al. 2009). Until recently, the potential of divergent selection to induce speciation in the presence of active gene flow was hotly debated. Contemporary biology holds that speciation can indeed occur in the presence of extensive gene flow between continuous, interbreeding populations as long as the drivers of disruptive selection are strong enough (Dieckmann and Doebeli 1999, Leblois et al. 2003, Benkman 2003, Rueffler et al. 2006, Rova and Björklund 2012).
In the scenario that follows, changing environmental conditions expose a population to strong divergent selection that leads to speciation. Initially, the population occupies the left lobe optimum of Figure 5a, at temperature T1. The dissection of the three-dimensional eco-phenotypic surface along four temperature values (Figure 5a) produces a set of two-dimensional fitness graphs (Figure 5b). Figures 5bI to 5bIV present the chronological order of the speciation scenario. In Figure 5bI, the peak in color represents the phenotypic distribution of the initial population; the other two fitness peaks are vacant. A series of cold winters forces the population to undergo adaptive change (Figure 5bII, 5bIII) that leads to the evolutionary bottleneck of 5bIV (T4). After that point, a climatic rebound to warmer temperatures triggers a ‘dimple’ or ‘split of peaks’ speciation scenario (Rozenzweig 1978) as in 5bV and a separated population will hence occupy the intermediate fitness peak (5bVI and 5bVII). The newly occupied peak corresponds to the right lobe of the horseshoe-shaped eco-phenotypic landscape (Figure 5a).
To sum up, this model shows that a horseshoe shaped eco-phenotypic landscape may have a special significance for sympatric speciation in continuous populations. However, the shape of the eco-phenotypic landscape is not a sufficient condition for sympatric speciation. The pace and amplitude of environmental oscillations, the strength of selection, the covariance with other environmental and phenotypic characters and the genetic variance and covariance will all have to be accounted for before an accurate prognosis can be made. The strength of the eco-phenotypic landscape is that it retains its form over phenotypic or environmental changes and can serve as a template that allows for long term heuristic projections after the integration of the aforementioned parameters.
Fitness of hybrids: Ηeterosis and outbreeding depression [this part was excerpted from the paper’s published version]
Heterosis and outbreeding depression describe crossbreeding events where hybrid fitness is, respectively, enhanced or depressed in relation to their parental forms. In populations that have had enough time to adapt to their environments, outbreeding depression is the most usual of both cases since any change would shift them away from their local optima (Nosil et al. 2005). Heterosis can be expected in the rare event that an intermediate fitness peak occupies the space between parental populations (Mallet 2007).
The fitness of hybrids is commonly measured in their parental environments by reciprocal transplant and phenotypic manipulations techniques (Edmans 1999; Rhode and Cruzan 2005). These methods, albeit indispensible on the practical level, have been criticized as having a critical blind spot. Hendry (2015) has noted that reciprocal transplants normally test hybrids and backcrosses in the parental environments, but those same hybrids and backcrosses would presumably have high fitness in intermediate environments. Thus, the experiments described above can’t reveal the presence of a fitness valley unless they also confirm the absence of intermediate environments. A similar line of argument is taken by Rundle and Whitlock (2001) who have highlighted the importance of determining the contribution of genetic and ecological mechanisms to hybrid fitness before any inferences concerning fitness valleys or speciation are to be made.
The following model presents a hybrid transplant experiment that could have leaded us to infer an adaptive valley for intermediate forms in what is actually an adaptive ridge. Consider the continuous population of Figure 3, where two parental forms (A and B) produce a hybrid form (H) which is assumed to be phenotypically intermediate. If we test the hybrid’s fitness in either of the parental environments, the outcome would be a significant fitness depression (fitness=0 in the graph) leading us to infer a fitness valley. However, in the intermediate environment the hybrid’s fitness would be equal or higher than the parental forms, indicating the presence of a continuous adaptive ridge (Rieseberg et al. 2003).
In vivo, the convergence of parents and the upbringing of their offspring in an intermediate environment provide a plausible physical mechanism for heterosis. Evidently, the shape of the eco-phenotypic landscape will play a defining role: A horseshoe of the likeness of Figure 5 is more likely to induce outbreeding depression than heterosis for intermediate forms. Overall, the eco-adaptive landscape may prove useful both for the conceptualization of naturally occurring hybridization processes and identification of the analytical scope of hybrid fitness experimental designs.
We decided to omit this latter part on heterosis from the published version of the paper, since one of the reviewers identified some weaknesses in this section. However, we are citing Ben Haller’s comment on this part for anyone wishing to take it up from here:
This is one place where I think you can actually go a bit further than you do, by pointing out that plotting experimental results on your proposed type of landscape plot would immediately make the error described by Hendry 2015 obvious; the graphical exercise would expose the conceptual flaw. And therefore everybody ought to use your diagrams when presenting such work. :-> You hint at that here, but don’t quite say it outright.
Lastly, here is Ben’s concluding comment for our paper, effectively describing an opening for future research:
In the end, I find that you didn’t go as far as I expected you to go. If you really want to fuse ecology and evolution, then you need to get into things like multispecies dynamics (how does one species affect the fitness landscape experienced by another species?), coevolutionary dynamics (how might two coevolving species be visualized using your sort of plots?), and eco-evolutionary dynamics (does that fit somehow into your scheme?).
Well, this is flattering, but I don’t think I can do that. It’s like asking from a high school physics teacher to fuse relativity with quantum mechanics. But I wish someone else does it; you will need someone who has spent a big part of their life in this, not just a passer-by who only stayed for a short while. From my part, I’m happy if I stirred some conversation. It is almost certain that I will never return to evolutionary biology for anything more than an occasional reading; it is not practical to invest more time in staying updated in a field as distanced from my own field. Also, from a career perspective, it does not make sense investing time for a publication in biology, then another in political science, another in epistemology (forthcoming). It needs a substantially greater effort to acquaint oneself with the body of knowledge and terminology of a new field each time, let alone to produce work that meets the standards of an academic publication. However, I can’t help being all over the place since I suffer from what I’m sure is a form of greed: I want too to explore, in depth, many different fields. You can call it shifting intellectual curiosity. Anyway, I want to thank you for having me here, especially Andrew. I feel that I’ve learned a lot out of this process. Science is cool. Keep it up!
Aarssen, L. 2017. The sapiens advantage. Ideas in Ecology and Evolution 10: 6–11.
Benkman, C. W. 2003. Divergent selection drives the adaptive radiation of crossbills. Evolution 57: 1176–1181.
Benkman, C. W. 2003. Divergent selection drives the adaptive radiation of crossbills. Evolution 57: 1176–1181.
Berner, D., Grandchamp, A. C., and A. P. Hendry. 2009. Variable progress toward ecological speciation in parapatry: stickleback across eight lake-stream transitions. Evolution 63: 1740–1753.
Dieckmann, U. and M. Doebeli. 1999. On the origin of species by sympatric speciation. Nature: 400 (6742): 354.
Edmands, S. 1999. Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53:1757–1768.
Hendry, Α. 2016. Eco-evolutionary dynamics. Princeton university press
Hendry, A. P., Bolnick, D. I., Berner, D., and C. L. Peichel. 2009. Along the speciation continuum in sticklebacks. Journal of Fish Biology 75: 2000–2036.
Kirkpatrick, M. and N. H. Barton. 1997. Evolution of a species' range. The American Naturalist 150: 1-23.
Leblois, R., Estoup, A., and F. Rousset. 2003. Influence of mutational and sampling factors on the estimation of demographic parameters in a “continuous” population under isolation by distance. Molecular biology and evolution 20: 491–502.
Mallet, J. 2007. Hybrid speciation. Nature 446: 279-283.
Nosil, P., Vines, T. H., and D. J. Funk. 2005. Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59: 705-719.
Rhode, J. M., and M. B. Cruzan 2005. Contributions of heterosis and epistasis to hybrid fitness. The American naturalist 166: 124–139.
Rieseberg, L. H., Raymond, O., Rosenthal, D. M., Lai, Z., Livingstone, K., Nakazato, T. et al. 2003. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301 (5637): 1211-1216.
Rozenzweig, M.L. 1978. Competition speciation. Biol. J. Linn. Soc. 10: 275–289.
Rousset, F. 2000. Genetic differentiation between individuals. Journal of Evolutionary Biology 13: 58–62.
Rova, E., and M. Björklund 2012. The influence of migration on the maintenance of assortative mating. Animal Behaviour 83(1): 11-15.
Rueffler, C., Van Dooren, T. J., Leimar, O., and P. A. Abrams. 2006. Disruptive selection and then what? Trends in Ecology & Evolution 21: 238–245.
Rundle, H. D., and M. C. Whitlock. 2001. A genetic interpretation of ecologically dependent isolation. Evolution 55(1): 198-201.