Wednesday, January 18, 2012

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.

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

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.

Thursday, January 5, 2012

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!

Monday, January 2, 2012

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

A 25-year quest for the Holy Grail of evolutionary biology

When I started my postdoc in 1998, I think it is safe to say that the Holy Grail (or maybe Rosetta Stone) for many evolutionary biologists w...