Download Which ecologically important traits are most likely to evolve rapidly?

Oikos 118: 12811283, 2009
doi: 10.1111/j.1600-0706.2009.17835.x,
# 2009 The Author. Journal compilation # 2009 Oikos
Subject Editor: Per Lundberg. Accepted 2 April 2009
Which ecologically important traits are most
likely to evolve rapidly?
John N. Thompson
J. N. Thompson ([email protected]), Dept of Ecology and Evolutionary Biology, Univ. of California Santa Cruz, Santa Cruz, CA
95064, USA
The Origin of Species was as much an ecological treatise as
it was an evolutionary treatise. Darwin argued that natural
selection favored adaptation to local physical and biotic
conditions, which led to the divergence of populations
living in different environments. In his view, evolution was
an ongoing ecologically driven process. Yet a hundred and
fifty years later much research in ecology continues to be
based on the view that we can make a distinction between
ecological time and evolutionary time. We often proceed as
if the genetic structure of species remains constant, allowing
us to ignore the potential for ongoing rapid evolution as we
study the processes shaping the dynamics of populations,
communities and ecosystems.
The fact that so much important ecological research can
continue to be done without even a nod to the potential for
ongoing evolution suggests that there must be at least some
truth to that assumption. The question is, how much truth?
Can we be sure that we are capturing the actual mechanisms
of ecological dynamics when we carry out studies that do
not attempt to evaluate whether any of the observed
dynamics are due to rapid evolutionary change? Surely by
this stage in our science we should be able to state that, in
general, ongoing rapid evolution accounts for, say, less than
five percent or, at the other extreme, more than fifty percent
of the ecological dynamics we observe in populations or
communities during time spans of several decades or
centuries. But we cannot do that, and it should worry us
as scientists because evidence continues to accumulate of the
ongoing evolution of populations over these short time
spans. Currently, each of us guesses whether to include
evaluation of rapid evolution in our ecological studies, and
we design our studies based on those guesses.
Part of the problem is that we lack a sense of which
ecologically important traits are likely to evolve very quickly
in ways that affect short-term ecological dynamics and
which are likely to evolve slowly in ways that have little
immediate effect. We have hundreds of studies of rapid
evolution in contemporary time but also scores of studies of
stasis in morphology of some fossil species over millions of
years. In between these two extremes, we have studies
showing rapid evolution under some ecological conditions
but no apparent evolution under other conditions. We lack
a sense of the proportion of ecologically important
evolutionary changes that are very fast, moderately fast, or
very slow.
If we assume that evolution is relatively consistent across
all traits, then we would expect to find little evidence in
nature of stasis in traits. Yet we know that many traits, such
as bilateral symmetry or restriction to marine environments,
are highly conserved within lineages. If instead we assume
that traits are highly variable in their evolvability, then rapid
evolutionary dynamics and stasis should be clearly evident
within and among taxa, and that is what we see. We do not
know, though, how linear, non-linear, or steep is the shape
of that distribution (Fig. 1). Just as importantly, we
currently lack sufficient data across a broad range of traits
and taxa to undertake a convincing analysis in a systematic
way.
If the shape of the distribution is highly non-linear, then
the role of rapid evolution in contemporary ecological
dynamics may be limited generally to a small number of
traits. If we knew that to be true, then we could focus on
those traits when assessing the role of rapid evolution in
ecological dynamics. It would help solve the problem we all
encounter when we consider how to incorporate an analysis
of rapid evolution into ecological studies which traits
should we initially include in a study when we all have
limited time and money? Just as ecosystem biologists need
to decide a priori which nutrients, micro-nutrients, climatic
variables, and water or soil properties to monitor during an
experiment, population and community ecologists need to
develop better a priori decisions on which traits to monitor
when assessing rapid evolution during an ecological study.
For now, we tend to include a few morphological,
physiological, or behavioral traits that we think might be
important to adaptation of a population in that physical or
biotic environment, but we generally make that choice in a
vacuum of knowledge of the likely evolvability of those
traits relative to other traits.
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Number of traits
Evolutionary rates
Figure 1. Alternative views of the distribution of evolutionary
rates of traits important to population, community, or ecosystem
dynamics, expressed on a linear scale of rates. The assumption in
this figure is that more traits evolve slowly than quickly, but
hump-shaped distributions are also plausible.
We can draw on the growing number of very useful and
up-to-date published summaries, reviews, and meta-analyses of phenotypic selection or rapid evolution (Fussman
et al. 2007, Carroll 2008, Kingsolver and Pfennig 2008,
Darimont et al. 2009) but we do not know the extent to
which those traits are actually representative of the traits we
should have studied. As has been noted repeatedly, most
studies of phenotypic selection and rapid evolution are still
on morphological traits, although analyses of rapid evolution of physiological and biochemical traits are increasing as
more studies have evaluated population responses to climate
change or emerging diseases. We still have very few studies
on more subtle traits that are potentially important to the
overall structure and dynamics of the web of life, such as
rapid evolution of preference hierarchies for different host
or prey species. These hierarchies affect which species
interact with one another and how species coevolve with
each other. Evaluating rapid evolution of relative preferences is inherently harder than evaluating the evolution of
lengths, widths, or titer levels. But we need a better
understanding of the relative evolvability of preference
hierarchies because even slight evolutionary changes in these
hierarchies could have large effects on the ecological
structure and dynamics of the web of life.
In general, then, we need studies of the relative
evolvability of the full range ecologically important traits,
especially subtle ones that can alter the ecological and
coevolutionary links among species. These studies will put
us in a better position to decide on which traits to include
when we are trying to evaluate the role of rapid evolution in
ecological dynamics. Collectively, such studies will also tell
us whether the distribution of evolutionary rates is highly
non-linear rather than linear, or even hump-shaped, among
ecologically important traits. Knowing that, we can then ask
whether the traits most likely to evolve quickly are also the
ones most likely or least likely to affect population,
community, and ecosystem dynamics. It could be that,
despite the accumulating evidence of ongoing rapid evolution in some traits, much of that evolution simply is not
important in ecological dynamics. Alternatively, it could be
that selection and local adaptation on highly evolvable traits
is precisely what keeps populations and species in the
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ecological game over even moderate periods of time. Those
rapidly evolving traits may not necessarily be important in
speciation or the higher level diversification of taxa, but they
may be the traits that keep populations around long enough
for selection to act on other traits that do affect speciation.
Studies of the relative evolvability of ecologically
important traits will also tell us whether the form of
selection varies along the continuum from fast-evolving to
slow-evolving traits. Measuring traits in darwins change in
a trait by a factor of e in a million years places the
emphasis on changes in means during evolution, whereas
the continued evolution of the variance of traits may be
equally important in ecological dynamics. Perhaps the
greatest role of rapid evolution in ecological dynamics is
through stabilizing selection that keeps the variance in traits
in check within population. Or perhaps its greatest role is
through negative frequency-dependent selection, which,
within certain bounds, continually favors rare genetic forms
within populations.
Kingsolver and Pfennig (2008) recently puzzled over
why more populations do not appear to reside at adaptive
peaks, and why studies of phenotypic selection indicate that
disruptive selection may be as common as stabilizing
selection. They noted that adaptive peaks may be constantly
changing and suggested competition for resources as one
potential driving force. Or course, the ‘resources’ are often
other species and those species evolve, sometimes rapidly, in
response to exploitation. The process of coevolution itself
may therefore continually change the adaptive landscape of
interacting species at least for the suite of traits that affect
the outcome of an interaction. One of the things we have
learned through studies of the geographic mosaic of
coevolution in recent years is that interacting species
continually evolve in different ways in different ecosystems,
and may evolve in different ways over time even in the same
ecosystem, with changes sometimes observable on the time
scale of just hundreds of years or decades (Thompson
2009).
An increased emphasis on studies of the relative
evolvability of traits will also tell us whether the background
rate of ecologically important evolution is low or high. If
almost all rates are low, then cases of rapid evolution can be
treated as interesting exceptions. We can focus on whether
these instances of rapid evolution become either damped
across generations or, occasionally, shift populations and
communities to new equilibrium states. It seems unlikely,
though, that the background level of ecologically relevant
evolution is low. The number of examples of rapid
evolution has now grown so large that it is difficult to
maintain the view that the background level of rapid
evolution in ecologically important traits is low, especially
as we learn more about microbial populations, fungal and
bacterial populations, and life in general beyond vertebrates.
After a hundred and fifty years since the publication of
The Origin of Species, we should be able to do better than
now in evaluating the role of rapid evolution in population,
community, and ecosystem dynamics. We have the tools
today to do it, and the importance of doing so grows each
year as we continue to impose potentially strong selection
pressures on all the earth’s major ecosystems.
References
Carroll, S. P. 2008. Facing change: forms and foundations of
contemporary adaptation to biotic invasions. In: Conservation biology: evolution in action. Blackwell, pp. 361372.
Darimont, C. T. et al. 2009. Human predators outpace other
agents of trait change in the wild. Proc. Natl Acad. Sci. USA
106: 952954.
Fussman, G. F. et al. 2007. Eco-evolutionary dynamics of
communities and ecosytems. Funct. Ecol. 21: 465477.
Kingsolver, J. G. and Pfennig, D. W. 2008. Patterns and power of
phenotypic selection in nature. Bioscience 57: 561572.
Thompson, J. N. 2009. The coevolving web of life. Am. Nat.
173: 125140.
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