- Top of page
- Selection in variable environments
- Adapt or die
- Life in the new atmosphere
- Literature cited
We discuss three interlinked issues: the natural pace of environmental change and adaptation, the likelihood that a population will adapt to a potentially lethal change, and adaptation to elevated CO2, the prime mover of global change.
1. Environmental variability is governed by power laws showing that ln difference in conditions increases with ln elapsed time at a rate of 0.3–0.4. This leads to strong but fluctuating selection in many natural populations.
2. The effect of repeated adverse change on mean fitness depends on its frequency rather than its severity. If the depression of mean fitness leads to population decline, however, severe stress may cause extinction. Evolutionary rescue from extinction requires abundant genetic variation or a high mutation supply rate, and thus a large population size. Although natural populations can sustain quite intense selection, they often fail to adapt to anthropogenic stresses such as pollution and acidification and instead become extinct.
3. Experimental selection lines of algae show no specific adaptation to elevated CO2, but instead lose their carbon-concentrating mechanism through mutational degradation. This is likely to reduce the effectiveness of the oceanic carbon pump. Elevated CO2 is also likely to lead to changes in phytoplankton community composition, although it is not yet clear what these will be.
We emphasize the importance of experimental evolution in understanding and predicting the biological response to global change. This will be one of the main tasks of evolutionary biologists in the coming decade.
Global change presents a clear, immediate and urgent challenge for evolutionary biology. The transformation of environments by agriculture and industry has created, and continues to create, a wide range of unintentional experiments in which populations are exposed to severe and novel perturbations, and either adapt to them or cease to exist. The greatest of these experiments is now under way: the alteration of the atmosphere and climate of the Earth, with consequences for every living thing. In this opening article of a new journal, we shall not attempt to offer a review of the whole field, which would be too intricate and extensive to fit within the confines of a short paper. We shall instead try to sketch the main tasks that we think that evolutionary biologists should undertake to contribute to our understanding of the future. Our account is organized into three sections. The first deals with the variability that is commonly experienced by natural populations, and how they respond to it. The second is concerned with whether or not populations can adapt to a novel and severe stress before being extinguished by it. The final section describes how phytoplankton populations may adapt to the prime mover of change, the increase in atmospheric concentration of carbon dioxide. The emphasis throughout is quantitative and experimental. We hope, and we believe, that evolutionary biology is the key to predicting how the world will change, and we see this as the principal task of evolutionary biologists in the next few decades.
Life in the new atmosphere
- Top of page
- Selection in variable environments
- Adapt or die
- Life in the new atmosphere
- Literature cited
The environmental factor that is driving potentially stressful change is not in itself stressful at all: elevated CO2 is unlikely to represent a lethal stress to any organism, and will actually increase the growth of green plants and algae. It is likely to alter the species composition of communities, however, and some species may become extinct as a consequence. Moreover, shifts in composition, together with the evolution of individual species, may alter whole-community properties such as primary productivity. There is an urgent need to understand how populations and communities will respond to elevated CO2, because the atmosphere is changing so rapidly: there has been an increase in atmospheric CO2 of approximately 90 ppm since the beginning of the industrial revolution, with the largest increase occurring during the past century (see for example Watson et al. 2001). Phytoplankton organisms can evolve in response to global change because they reproduce quickly relative to the timescale of global change and have large populations, so that future populations may be genetically different from contemporary ones. Here, we review selected examples of how experimental evolution can be used to advance understanding of how phytoplankton communities may respond to increases in atmospheric CO2 over the next few decades.
The oceanic carbon sink
Although the potential for adaptation to atmospheric change is an interesting issue, and one that will surely be used as a model system to make advances in general theory, the main reason for our interest in phytoplankton responses to elevated CO2 is pragmatic: there is a potential carbon sink in the ocean, and we would like to be able to make predictions about it. About one-half of all photosynthetic carbon fixation on the planet occurs in oceans (Falkowski 1994; Beardall and Raven 2004). Phytoplankton have the potential to absorb a portion of anthropogenic CO2 as fixed organic carbon and trap it in deep ocean sediments (Sarmiento and Toggweiler 1984; Raven and Falkowski 1999; Schippers et al. 2004), although debate exists over the size of such a sink. The biological carbon sink has generated interest in terms of its possible role in slowing global CO2 enrichment, and has given rise to large-scale experiments designed to increase phytoplankton blooms and subsequent C sinking by adding iron dust to sections of ocean (Boyd et al. 2000; Buesseler et al. 2004; Coale et al. 2004). Although some increase in phytoplankton biomass has been observed, it has been difficult to assess how much carbon was exported to deeper waters, and in the two cases where carbon export was reported, it was modest compared with expected levels (de Baar et al. 2005). Experiments like this show continued interest in the idea that phytoplankton may have the potential to help manage global CO2 enrichment.
Experimental evolution will enable us to make predictions about the carbon cycle that have clear ecological and economic value. To study a simple version of this in terms of the biological carbon pump, we need two pieces of information: which species will be present, and how much carbon will they sink? In other words, what will be the future composition of phytoplankton communities, and will descendents of individual species (or functional groups) continue to take up carbon at the same rate as contemporary taxa?
The evolved high-CO2 syndrome
Carbon uptake in model phytoplankton species is relatively well understood (see Raven 1991; Beardall et al. 1998; Riebesell 2004 for reviews). Progress continues to be made in documenting carbon uptake and growth in other species that are thought to play an important role in marine carbon fixation (for example Fu et al. 2007; Hutchins et al. 2007; de Castro Araújo and Garcia 2005; Bidigare 2002). Most recent studies, including those just cited, tend to report responses to changes in carbon availability coupled with other environmental change (see for example Schippers et al. 2004). While detailed physiological work can tell us a great deal about how phytoplankton respond to short-term increases in carbon availability, either alone or as part of a more complex environmental change, there is ample evidence that these responses are not reliably maintained over longer timescales (Polle et al. 2001; Collins and Bell 2004).
Most ecological and evolutionary theory is framed in terms of adapting to scarcity or stress. In contrast, contemporary global change is characterized by nutrient enrichment. Marine phytoplankton are not typically CO2 limited for growth, in part because most actively transport carbon into the cell using an inducible carbon-concentrating mechanism (CCM) (Badger et al. 1998; Sültemeyer 1998; Badger and Spalding 2000; Coleman et al. 2002). The CCM tends to be tightly regulated such that it is downregulated when CO2 is abundant (Bozzo and Coleman 2000). Information about the presence and affinities of CCMs is vital to determining how much carbon algal populations take up under a given CO2 regime. Here, experimental evolution can help to understand whether CCMs will continue to be maintained in their current state, and from this, how stable we expect the CO2 affinity and rate of carbon uptake of phytoplankton to be over long timescales. This directly addresses the question of how closely we expect future phytoplankton populations to resemble contemporary ones.
To identify the long-term response to elevated CO2,Collins and Bell (2004) cultured the unicellular alga Chlamydomonas reinhardtii for 1000 generations at concentrations of CO2 that gradually increased from ambient values to 1000 ppm.
We found that the lines evolved a syndrome characterized by increased photosynthesis without increased growth or insensitivity of both growth and photosynthesis to elevated CO2 (Collins and Bell 2004). Microalgae isolated from the soil around naturally occurring CO2 springs expressed a similar phenotype (Collins and Bell 2006), strengthening the case that the laboratory selection experiment could be used to predict the response of natural populations. The evolved syndrome is contrary to the short-term response of C. reinhardtii to elevated CO2, which involves an increase in both photosynthesis and growth. Hence, the evolutionary responses differed in both direction and magnitude from physiological responses. It follows that the predicted net CO2 uptake of future phytoplankton communities is 38% less than the value expected from contemporary populations held under the same elevated CO2 conditions, when the evolutionary response is taken into account (Collins et al. 2006) (Fig. 5). Moreover, there was significant divergence between initially similar replicates, showing that physiological responses are unlikely to remain constant or to scale up predictably over hundreds of generations. The statement that short-term responses may not scale up predictably to longer timescales is hardly surprising or novel, and studies such as these highlight the need for experimental tests of evolutionary responses to elevated CO2 in marine phytoplankton. Long-term selection experiments with diatoms, coccolithophores and cyanobacteria are feasible, although more cumbersome than those with Chlamydomonas, which grows faster and reaches greater densities.
Figure 5. Affinity of net total carbon uptake, shown as K0.5 in wild-type and high selection (numbered) lines acclimated to 1050 ppm CO2 (filled bars, H) and air (white bars, A). Net total carbon uptake was calculated as bicarbonate uptake + net CO2 uptake). Each bar represents averages ± standard error of the mean from independent duplicate or triplicate measurements. Accompanying table shows effect of changes in carbon uptake rates and population size on carbon sink calculations. From Collins et al. (2006).
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The main outcome of selection at elevated CO2 in our experimental lines of Chlamydomonas was the degeneration of a regulated CCM (Collins et al. 2006). There was neither a fitness cost nor a benefit to the degeneration of the CCM, nor to the loss of its regulation at high CO2, suggesting that the pathway simply deteriorated through the accumulation of conditionally neutral mutations. Studies of pathway degeneration in yeast (Sliwa and Korona 2005; Maclean 2007) are consistent with unused or unnecessary pathways being lost by mutation accumulation, although there is also ample evidence that unused pathways are often maintained, perhaps because they are tightly regulated and do not incur a metabolic cost when they are not in use (Maclean 2007).
Understanding how CCMs might change in response to elevated CO2 is further complicated by the biology of marine phytoplankton growth. As marine phytoplankton form blooms that may locally deplete CO2 supplies, the loss of a regulated CCM may be deleterious in natural populations even if global levels of CO2 rise. In this case, the CCM might be maintained by periodic strong selection, even though experiments done at constant high CO2 predict its degradation. To make an educated guess on whether carbon uptake will be maintained in its current form by purifying selection, more realistic experiments incorporating nutrient fluctuations seen in bloom-bust growth cycles are needed.
The effect of elevated CO2 on community composition
There have been several attempts to investigate how high CO2 levels may affect community composition. Some studies have tested the hypothesis that an important response to CO2 enrichment will be species succession, based on competition between two or more species with different resource requirements (Burkhardt et al. 2001; Rost et al. 2003). The findings from short-term enrichment studies on natural phytoplankton assemblages have been equivocal, depending on the initial assemblage used and the duration of the study (Tortell et al. 2000, 2002). While there is still debate about whether phytoplankton will respond to CO2 enrichment by increasing growth or photosynthesis rates, phytoplankton usually have some other response to elevated CO2, such as changes in calcification, nitrogen use, or the productions of extracellular polymers (Beardall et al. 1998; Clark and Flynn 2000). Here, microcosm studies can be used to ask how increasing CO2 may change more complex community dynamics. Shikano and Kawabata (2000) investigated the effect of elevated CO2 and nutrient levels on a model community made up of Escherichia coli (bacteria), Tetrahymena thermophila (ciliate) and Euglena gracilis (green flagellate). This work showed differences in community composition that were both directly and indirectly attributable to elevated CO2. The main effect of CO2 enrichment in this system was an increase in algal biomass. This was correlated with several indirect effects, most notably a reduction in bacterial biomass, which is the opposite effect from CO2 enrichment in pure cultures of E. coli. Interestingly, the indirect effects of CO2 enrichment were not observed to the same extent, or even in the same direction, if concentrations of other nutrients were not also increased. This shows how elevated CO2 and nutrient levels may affect dynamics in a specific community.
Recent studies in experimental evolution have begun to address the effects of ecological processes on evolutionary outcomes. For example, natural enemies retarded the diversification of microbial systems whose diversity was high in the absence of the enemy by reducing population size (Morgan and Buckling 2004; Meyer and Kassen 2007). However, the opposite effect occurred in cases where diversity was low in the absence of an enemy (Gallet et al. 2007). These sorts of studies can help to establish general principles that will help to reconcile the apparent contradictions between studies documenting community-level responses to environmental change, including elevated CO2.
Adaptation and the rate of global change
In the studies we have described, experimental evolution overlaps with shorter-term studies involving phytoplankton responses to global change. There are, however, some noteworthy issues that experimental evolution is uniquely equipped to study. One of the most obvious features of contemporary global change is that the increase in CO2 is much more rapid than in the geological past. While it seems clear that rates of environmental change should have a systematic effect on evolutionary outcomes, there is little explicit discussion of how this may occur. Both short-term (physiology) and long-term (evolution) experiments typically begin by suddenly placing a population in a stressful environment. The population is then allowed to either acclimate (reach some sort of steady-state physiological response) or adapt (reach some sort of steady-state evolutionary response). By contrast, global change is occurring gradually, so that populations will experience a continuous range of intermediate environments. A few simulation studies have made testable predictions about the effect of constantly changing environments on adaptive outcomes, in particular that lower rates of environmental change affect the dynamics of adaptive walks by reducing the fitness effect of fixed beneficial mutations, and increasing the range of time where the substitutions of largest effect are likely to occur. In addition, adaptation to slower rates of environmental change results in fewer possible outcomes relative to lineages that adapt to a sudden change (Collins et al. 2007; Kopp and Hermisson 2007). These simulations are in good agreement with mathematical models quantifying the lag with which a population is able to track a changing environment (Waxman and Peck 1999; Broom et al. 2003). At present, there are no published experimental tests of these hypotheses. Understanding how rates of environmental change affect evolutionary outcomes will help interpret laboratory experiments, where environments must be changed much faster than natural environments, and to use historical data more effectively, where rates of global change were many orders of magnitude slower than contemporary climate change.
From the above studies, how can experimental evolution help us to make predictions, or at least educated guesses, about future populations of phytoplankton and how much carbon they may sink? Based on the sparse experimental data, it is likely that phytoplankton will evolve in response to elevated CO2. The direct evolutionary response may not be adaptive, however, and may instead result in populations that are less productive than their ancestors. It is likely that rising CO2 will also cause changes in phytoplankton community composition. Although there are predictions as to what these changes might be (Rost et al. 2003), they have yet to be tested using assemblages that have had the opportunity to undergo both ecological interactions and evolutionary change. At present, we are not in a position to make an informed guess about the composition of future phytoplankton communities, nor do we know how competitive interactions may alter the evolutionary response to elevated CO2.
The main practical limitation to understand microalgal evolutionary responses to global change is simply the lack of published studies. There is no basis for determining how much variation in evolutionary responses is likely to exist within or between taxa. Work in terrestrial systems near CO2 springs suggests that long-term responses vary idiosyncratically within or between taxa (Bettarini et al. 1999), whereas in microalgal communities at the same springs different genera responded in much the same way (Collins and Bell 2006).
Although detailed natural history information is needed to understand how the biology of particular taxa may change, there are also aspects of general evolutionary theory relevant to understanding the likely effects of global change on phytoplankton populations. As one of the important effects is likely to be a shift in the taxonomic composition of phytoplankton communities, it will be necessary to understand how ecological processes such as competition and predation affect evolutionary outcomes. This research program is well-advanced, and general patterns are already beginning to emerge (Brockhurst 2007). A second area where advances in general theory will help is in expanding our understanding of adaptation to accommodate more complex environmental change, such as constantly changing environments or scenarios where several aspects of the environment change simultaneously. Our current basis for understanding adaptation is most useful when a large, well-adapted population is subjected to a sudden change, and then allowed to adapt to a stable environment. While this is often a useful and sufficient simplification, it does not allow us to learn as much as possible from historical data or laboratory experiments that investigate responses to global change.