Why should we care about rapid evolution?

            In this, my first post on this blog, I wanted share how I came to study Eco-Evolutionary Dynamics. My journey grew from a passion for understanding the process of evolution to experimentally testing its impact.

            In a growing number of natural systems, evolution has occurred so quickly that scientists can observe it. Examples of such “rapid” or “contemporary” evolution have been observed in all major lineages and are driven by natural, sexual, and artificial selection. When I heard of such studies I knew that this would be the focus of my doctoral studies, which I undertook in a US lab at the forefront of such work. My first dissertation committee meeting, however, did not go as planned.

            While expressing my desire to experimentally study rapid evolution in the field, one committee member (Dr. Derek Roff) said something along the lines of: “We know rapid evolution occurs and the mechanism causing it so why should we care rapid evolution occurs?” Initially I reacted like many scientists do when faced with criticism about their area of focus: I assumed that he didn’t understand the topic. I soon came to realize that he had a valid point and one that has received much less attention in Evolutionary-Ecology: How does rapid evolution alter our understanding of other biological processes? Should ecologists, specifically, care about rapid evolution? This became the focus of my dissertation.  

            I discovered that other biologists had begun investigating how rapid evolution influences ecological dynamics (especially David Pimentel in the 1960s). Yet the pervasive notion in ecology was that evolution could be ignored unless one was studying patterns over millions of years. This idea is expressed most often as a supposed dichotomy between Ecological and Evolutionary timescales. This separation has its roots in Darwin’s assertion that evolution is a slow and gradual process. Rapid evolution, however, is now known to sometimes occur within a few generations, creating an opportunity for the evolution of populations to change short-term ecological processes.

            To study the impact of rapid evolution on ecological dynamics, I decided to use experimental evolution. The basic approach was to create replicated populations that can or cannot evolve by manipulating genetic variation. Inspired by the studies of David Pimentel and Nelson Hairston Jr., I wanted to break new ground by taking this experimental approach into the field. Despite being in a fish evolution lab, I decided to develop my own study system: green peach aphids.

            My focal study population is found on a small nature reserve in Southern California. I collected aphids and genetically identified clonal lineages. Using population growth experiments, I identified clones that differed by up to 17% in exponential growth rate. I now had the variation required to conduct experimental evolution.

            I first tested whether rapid evolution impacts ecology under controlled greenhouse conditions. I created replicate populations of aphids that had either a single aphid clone (no genetic variation and hence no evolution was possible) and compared these to populations with two different aphid clones (genetic variation in fitness and hence evolution was possible). I then let the aphid populations grow on their mustard host, and counted them twice a week for one month (4-5 generations). An ecologist predicting population growth would simply use the average exponential growth rate in each population (which is the same on the first day as any day). However, my results showed that populations with genetic variation grew up to 34% faster than predicted using mean growth rate! Genotyping confirmed that this was because evolution occurred in the two-clone treatments. Aphid clones changed in frequency, increasing the population growth rate within the time course of population expansion. These results suggest that to properly predict population dynamics one might need to explicitly account for evolutionary change.

            A more difficult question to address is whether such effects could occur in nature in the face of environmental variation and the presence of other species. I thus returned to the nature reserve and conducted a similar experiment. I created replicated aphid populations in the field, some of which could evolve and others which could not. I also covered half the populations with cages whereas the other half were not caged and thus competitors, predators, and parasitoids could interact with the aphids. After one month, I found that evolving populations grew significantly faster, up to 42%, and reached up to 67% higher densities compared to non-evolving controls, even in the face of environmental variation. Interestingly, this effect only occurred in the natural uncaged treatments, highlighting that ecological context (e.g. predation and levels of competition) alters the strength of eco-evolutionary dynamics.

            These experiments showed that rapid evolution can impact population dynamics within only a few generations – but are these ecological changes feeding back to evolution, so-called Eco-Evolutionary Dynamics? I tested this idea, in the greenhouse, by manipulating not only the occurrence of evolution but also initial population density. Many interesting results were observed. Initial aphid density altered the rate and outcome of evolution. Density also quantitatively and qualitatively altered how rapid evolution impacts population growth rate, sometimes accelerating and sometimes decelerating growth. This experiment showed that one must account for density, population growth rate, and rapid clonal evolution to properly predict ecological and evolutionary outcomes.

            After many years of research and lots of counting, I have developed an even greater appreciation for evolutionary biology. Not only is rapid evolution cool, but it can be tremendously important and seems to strongly influence ongoing ecological processes. Changes in exponential growth rates that I have observed could have large impacts on community and ecosystem processes (but I need to test these effects more rigorously). Other study systems are starting to quantify how rapid evolution impacts higher levels of biological organization, and they are generating very interesting results. This is an exciting time for evolutionary-ecologists as the integration between ecology and evolution is leading to new insights and a deeper understanding of the natural world.

Martin M. Turcotte

University of Toronto at Mississauga

  

Motte-Rimrock Nature Reserve in Perris, CA

Experimental aphid population on an Hirschfeldia incana plant in the field

Turcotte, M.M., Reznick, D.N. & Hare, J.D. Experimental Assessment of Rapid Evolution on Population Dynamics. 2011. Evolutionary Ecology Research, 13, p. 113-131.

    http://www.evolutionary-ecology.com/v1.html

Turcotte, M.M., Reznick, D.N. & Hare, J.D. The Impact of Rapid Evolution on Population Dynamics in the Wild: Experimental Test of Eco-Evolutionary Dynamics.  Ecology Letters, 14(11), p. 1084-1092.  DOI: 10.1111/j.1461-0248.2011.01676.x

    http://onlinelibrary.wiley.com/doi/10.1111/j.1461-0248.2011.01676.x/abstract

Turcotte, M.M., Reznick, D.N. & Hare, J.D. Experimental Test of the Full Eco-Evolutionary Dynamic Cycle Between Rapid Evolution and Population Density. In Review.

Carnival of Evolution #43

  The 43rd Carnival of Evolution is now up at The EEB & Flow.  There's no post from us here at eco-evo/evo-eco this time around, but there are lots of other cool entries, so check it out.  We'll be back in the Carnival next month – December just kind of got away from us!

Evolutionary consequences of alewife divergence

As described in several posts on this blog, recent research has shown that evolutionary diversification (in species such as alewives and sticklebacks) can differentially impact ecological processes. Such work is important because it sets the stage for there to be an ongoing feedback between ecological and evolutionary forces within these systems. However, natural systems are inherently complex and genetic divergence in one organism, and associated ecological impacts of these changes, may alter the selective landscape and promote a series of evolutionary changes that propagate throughout the food web. The potential significance of such a ‘cascade of evolutionary change’ has been the focus of our recent research on interactions between populations of a fish predator, the alewife (Alosa pseudoharengus), and their zooplankton prey.

In lakes in Connecticut, the presence or absence of passages to the coastal ocean lead to lakes with anadromous alewives that migrate seasonally between marine and freshwater environments or lakes with permanent populations of landlocked alewives. Adult anadromous alewives migrate into lakes to spawn during each spring (March-May), and young-of-the-year (YOY) alewives spend ~6 months in freshwater before migrating back to the ocean each fall. In these lakes, large zooplankton, such as Daphnia, are abundant each spring, but are eliminated by alewife predation in early summer. Conversely, landlocked alewives are present in lakes year-round and, therefore the abundance of large zooplankton is consistently low. Previous work has shown that small-bodied zooplankton (i.e., Bosmina) dominate the zooplankton community in lakes with landlocked alewives and has promoted morphological divergence (gill raker spacing, gape size, preferred prey size) of landlocked alewife from anadromous ancestors.

Our first step was to determine if variation among these populations of alewives (and the ecological impacts of this variation) drive evolutionary divergence in their prey. We collected multiple populations of a single species of zooplankton (Daphnia ambigua) from lakes with anadromous and landlocked alewives (and also lakes without any alewife) and compared them for life history variation after several generations of rearing in a common environment. We found that Daphnia from lakes with anadromous alewife differ very strongly for many life history traits than Daphnia from lakes with landlocked alewife or no alewife. Furthermore, Daphnia from lakes with anadromous alewife typically displayed ‘higher fitness’ for the traits that were evaluated; they grew faster, developed more rapidly, and had larger clutches than Daphnia from lakes with landlocked lakes. The causal mechanism is likely related to variation in the annual migratory cycles of alewife and the known differences in lake seasonality. Daphnia in lakes with anadromous alewife are only present during the spring (when alewife predation intensity is low), and lakes in Connecticut are colder during the spring than summer. As a result, these evolutionary changes are best explained as an adaptation to a very short growing season and colder environment (i.e. countergradient variation) that are an indirect byproduct of intense seasonal predation by anadromous alewives.

We also explored the impact of alewife variation on the evolution of phenotypic plasticity in Daphnia. The presence of predators and the chemicals released by predators (kairomones) induce phenotypic changes in the life history, morphology, and behavior of prey. For instance, Daphnia typically develop faster and produce more offspring in the presence of fish chemical cues. A key requirement for the evolution of such plasticity is the existence of spatial and temporal environmental heterogeneity. Theory indicates that plasticity is favored when the environment is variable but predictable. In our lakes, landlocked alewives are present year-round, while anadromous alewives migrate predictably between marine and freshwater environments. Because these differences in migratory behavior have divergent impacts on Daphnia abundances, intraspecific variation in alewives may influence the evolution of plasticity in Daphnia. To explore this possibility, we reared Daphnia from lakes with and landlocked and anadromous alewives in the presence and absence of alewife chemical cues. This work revealed evidence for differences in plasticity among our focal populations of Daphnia. Daphnia from lakes with anadromous alewife responded much more strongly to the presence of alewife chemical cues for several life history traits (clutch size, size at maturation, growth, etc.) including the extent to which they engage in sexual reproduction (Daphnia alternate between asexual and sexual bouts of reproduction).

Overall, this research has revealed significant evolutionary consequences of intraspecific variation in alewives. The next step in this line of research is to determine if these evolutionary interactions between alewife and zooplankton have an ecological imprint in lakes.

Walsh, M. R., and D. M. Post. 2012. The impact of intraspecific variation in a fish predator on the evolution of phenotypic plasticity and investment in sex in Daphnia. Journal of Evolutionary Biology 25: 80-89

Walsh, M. R., and D. M. Post. 2011. Interpopulation variation in a fish predator drives evolutionary divergence in prey in lakes. Proceedings of the Royal Society B 278: 2628-2637

One from the Vault - Whither Adaptation?

I just attended the openning of the 2011 symposium of Andy's Gonzalez's Quebec Centre for Biodiversity Science (http://qcbs.ca/). Michael Donoghue gave a cool keynote talk to start things off about the importance of studying and understanding both rapid and slow evolution if we are to confront the current biodiversity crisis. This blog will have more to say about the meeting in a future post but something prompted me to do a quick post starting a new "One from the Vault" series.

Blogs like this one tend to focus on new events and papers but it is fun to dig up old ones too. This new "One From the Vault" series will highlight older papers both from our lab and from other researchers. The current installment - Whither Adaptation? - was inspired by Andy's comment when we met after Michael's talk that he was amazed that Michael had mentioned the two of us in the same sentence. The surprise was that our views are often so different that it would seem unlikely that we would be lumped together under a common theme. But it did happen one other time ...

Whither adaptation?

by: Andrew P. Hendry and Andrew Gonzalez*

Abstract: The two authors of this paper have diametrically opposed views of the prevalence and strength of adaptation in nature. Hendry believes that adaptation can be seen almost everywhere and that evidence for it is overwhelming and ubiquitous. Gonzalez believes that adaptation is uncommon and that evidence for it is ambiguous at best. Neither author is certifiable to the knowledge of the other, leaving each to wonder where the other has his head buried. Extensive argument has revealed that each author thinks his own view is amply supported by both theory and empirical evidence. Further reflection has revealed that the differences in opinion may start with the different disciplines in which we work: evolutionary ecology for Hendry and community ecology for Gonzalez. In the present paper, we each present devastating evidence supporting our own position and thus refuting that of the other. We then identify the critical differences that led to such opposing views. We close by combining our two perspectives into a common framework based on the adaptive landscape, and thereby suggest means by which to assess the prevalence and strength of adaptation.

*Each author thinks the other contributed less

Hendry, A.P., and A. Gonzalez. 2008. Whither adaptation? Biology and Philosophy 23:673-699.
http://www.springerlink.com/content/u741773914w3k2w7/

Carnival of Evolution #42

Carnival of Evolution #42 is now up at Ocelloid.  Enjoy!

Non-parallel evolution in Storrs and stickleback

Independent populations that colonize similar environments and then evolve similar traits provide strong evidence for a deterministic response to natural selection. The resulting pattern has been variously called “parallel” or “convergent” depending on similarity among the starting populations and on one’s preferred definition.*

As parallel evolution provides some of the most convincing evidence for the power of natural selection, finding it has become a rite of passage for evolutionary biologists working in any given natural system, and it is a common stamp of approval for authors publishing on adaptation. Over the years, I have probably seen more than a hundred papers that examine phenotypes from multiple populations in two or more environments. Some statistical model is applied to the data and the main effect of “habitat type” is examined with great expectation. When this effect is significant, the paper trumpets its success in documenting the power of natural selection in shaping the diversity of life.

What often strikes me about such papers, however, is that the population means of the different habitat types often overlap considerably. That is, some populations in one habitat type have larger traits values and some have smaller trait values than populations in the other habitat type. This pattern implies to me that the coarse classification of habitat type is, in reality, not very predictive of phenotype and that many other factors must also be involved. Sadly, investigators rarely embrace and explore – or even acknowledge – this unexplained variation. We recently published a paper* that does so, and I was prompted to make a blog entry about it as a result of my seminar visit last week to the University of Connecticut.

Parallel/convergent evolution was a common theme in discussions with many UConn folks. Some labs studied situations where different organisms occupy similar environments and so would be expected to evolve similar traits (Schlutz lab: adaptation to the osmoregulatory challenges of fresh versus salt water by stickleback and alewives). Other labs studied situations where similar body forms evolved independently and so one would expect similar selective pressures to have been the cause (Jockush lab: large and small bodied skinks of different lineages in California). In South Africa, the plant genus Pelargonium is highly variable in leaf shape and growth form (Schlichting and Holsinger labs). So variable, in fact, that I (as a non-plant person) would never have imagined that they would all be in the same genus. Presumably all of these different shapes and forms in Pelargonium are the result of adaptation to different environments, and yet species with very different growth forms can be found side-by-side in the same environment. (OK, I only saw them in a greenhouse but I am told this is true in nature.) If adaptation is the cause of this group’s radiation, then why are two plant types of very different form found in the same environment? This dramatic non-parallelism is just the sort of thing I am talking about.

To investigate non-parallelism, Renaud Kaeuffer, Dan Bolnick, Katie Peichel, and I quantified ecological (diet), morphological (body shape, trophic traits, armor traits), and genetic (neutral and QTL-linked microsatellites) variation in each of six independent lake and stream population pairs of threespine stickleback*. Some traits were remarkably parallel. For example, all lake populations had stickleback with shallower average body depths than did all stream populations (no overlap in the population means). Other traits, however, were decidedly non-parallel. For example, the main effect of habitat type (lake or stream) explained essentially none of the variation in armor traits. So what is the cause of this variation in parallelism? By relating divergence in morphological traits to the degree of ecological divergence, we were able to show that deviations from non-parallelism are mostly likely the result of variation in selection. That is, variation in parallelism is caused by selective factors that do not map so cleanly onto the coarse habitat type classifications that we (and possibly other investigators) typically use. We are not the first group to find this, of course, but we certainly have fun embracing it.

The pressing question to my mind is just how common and strong are these effects? How similar will be the physiological adaptation of alewives and stickleback? To what extent is the variation in skink body shape the result of adaptation to particular environments – as opposed to some other effect? Is the variation in growth form in Pelargonium the result of variation in microhabitats with a general location – or is it the result of some other historical contingency? To what extent does variation in gene flow cause deviations from parallel evolution. We previously found this last effect to be strong in lake and stream stickleback, and it also seems critical in Mark Urban’s salamanders.

Just how parallel is parallel evolution – and why?

Why natural selection will never cure the common cold!

In my last blog entry, I described a trip to Uppsala, Sweden, and the Beaver Snaps I drank there. I learned at the time that Beaver Snaps are often a northern Swedish speciality. This last week, I returned to Sweden – this time much closer to the land of Beaver Snaps. I was in Umea for their annual KBC days, an event where researchers from several departments at the university gather together to interact and share their research findings. My job was to give a plenary talk of general interest – and I spoke on Humans, Evolution, and the Future of Biodiversity. This was simply a grandiose title for what amounted to an advertisement for the importance of considering evolution when evaluating how human activities will shape future biodiversity. I also gave a research talk about ecological speciation.

The cool thing about trips like this is that you talk to all sorts of crazy people who have all sorts of crazy ideas. These ideas are sometimes useful and inspiring and sometimes not, but they are certainly always interesting. And sometimes these crazy ideas are what I remember most, such as in my “What did I learn today” entry from Belgium last winter. On this most recent trip, I spent some hours arguing about behavioural syndromes with my host Tomas Brodin – I remain to be convinced! And Lennart Persson espoused his paradoxical idea – they even have theory and data! – that increasing mortality on a given age class will increase the number and biomass of individuals in that age class. Already published in Science and PNAS, this theory is coming soon to a bookstore near you.

Now that stuff was bizarre enough but perhaps the most surprising discussion started with a question from someone who had seen my general talk. He wanted to know why natural selection has not eliminated our susceptibility to colds – after all they do make us damn miserable and we seem to get them all the time, particularly those of us with kids (more about this later). Now the usual answer to this question might be that colds are caused by micro-organisms that have very short generation times that allow them to adapt to us better than we can adapt to them. But I figure the more interesting answer is that colds don’t currently reduce our fitness – so selection won’t act to eliminate them. I certainly had a raging cold at the time and so the question stuck with me. I began to wonder if colds had actually reduced my reproductive success. I have two kids now but, without colds, would I have three – or four?

So clearly we need a study on this. Perhaps we should ask people whether or not they conceived their children when they had a cold. I suppose that would be hard to remember (hopefully so anyway) and so maybe we could instead test whether people that get more colds have fewer children. Better yet, we could experimentally induce colds in some bars and not others (that should be easy – we just infiltrate the dish washing staff) and then monitor mating and reproductive rates of the patrons (probably a bit harder). And, to figure out if sexual selection was the reason, we could take a bunch of people with colds, give some decongestants and not others, and send them into bars with instructions to ... well you get it. And why not take this train of thought to its logically absurd conclusion. I noted earlier that people with kids get more colds than do people without. Maybe this is a case of selection through sibling conflict. It clearly benefits the kids you already have if you don’t have more kids – because the available resources are divided to a lesser extent. So maybe, just maybe, colds are adaptive in children because they enable them to infect their parents thus (further) reducing the chance the parents will have more kids. Sick kids really are the birth control we always thought they were!



My first daughter, Aspen, trying hard to make sure I don't have a second daughter. It didn't work - perhaps because she couldn't have a cold all the time.