Andrew P. Hendry, "Evolutionary biology: The power of natural selection" (2005)

Evolutionary biology: The power of natural selection 

ANDREW P. HENDRY

Andrew P. Hendry is in the Redpath Museum and Department of Biology, McGill University, Montreal, Quebec H3A 2K6, Canada. 

e-mail: [email protected]

        Adaptation by natural selection is the centrepiece of biology. Yet evolutionary biologists may be deluding themselves if they think they have a good handle on the typical strength of selection in nature.

        The one constant in our world is change - change often wrought by our own devices. In consequence, some of the populations and species with which we cohabit have difficulty persisting. Yet organisms should be able to adapt to changing environments, as they have done for billions of years, diversifying into a bewildering array of environments. But extinctions are also a prominent feature of the past. Were these lost organisms unable to adapt to change? If so, are the rapid changes now being driven by humans too much for adaptation to combat? At the heart of these questions is the power of natural selection to bring about evolutionary adaptation in natural populations. Writing in Evolution, Joe Hereford and colleagues(1) bring this matter into stark relief.

        The primary mechanism of adaptive evolution is natural selection, whereby organisms possessing traits that improve their evolutionary 'fitness' - their survival and reproduction - contribute more genes to subsequent generations. Yet perceptions of the power of selection have recently swung at the end of a pendulum. Charles Darwin felt that "natural selection will always act very slowly, often only at long intervals of time, and generally on only a very few of the inhabitants of the same region at the same time"2. If Darwin was right, natural selection should be almost imperceptible, and adaptation must require "the long lapse of ages" (2). This perception held sway for more than a century before it was challenged by a series of empirical studies - most famously those showing dramatic changes in the coloration of peppered moths during industrialization (3). These studies inspired a wave of interest in actually measuring selection and adaptation in natural populations.

        By the mid-1980s, enough studies had accumulated for John Endler to profitably review them in his classic book Natural Selection in the Wild (4). Reviews of this sort typically collate and combine selection estimates for a variety of traits and studies so as to address general questions about the strength of selection (Box 1). Endler's review heralded a shift in our perceptions when he emphasized that "strong selection is not rare and may even be common"4, basing this conclusion largely on the observation that some studies documented quite strong selection.

        Another way to infer the power of selection is to actually measure evolutionary changes in natural populations5, 6. Studies taking this approach often document substantial changes over short time intervals, suggesting that natural selection does indeed have the power to drive rapid adaptation. Darwin was too modest, it seemed, about the power of his idea.

        Fast-forward to 1998, when I joined a discussion group led by Joel Kingsolver at the University of Washington. This group set about analysing all studies of natural selection published since Endler's book. Burdened by the practical needs of graduating, I soon bowed out of the project and did not see the results until 2001. Surprisingly, it seemed that Endler's conclusions had swung the pendulum too far back when Kingsolver et al. emphasized that "directional selection on most traits and in most systems is quite weak" (7). This conclusion was largely based on the observation that most estimates of selection were non-significant and centred around zero. A particularly worrisome finding was that most studies did not have sufficient statistical power to detect typical strengths of selection (7, 8). Perhaps the pendulum should swing all the way back to Darwin: natural selection really is weak in nature, except in exceptional situations.

        Enter Hereford et al. (1), who argue that previous reviews did not have objective criteria by which to judge whether selection was weak or strong. They suggest that this problem can be resolved if selection estimates for individual traits are standardized to allow comparison with the expected strength of selection on fitness itself (Box 1). Selection on fitness, they argue, provides a clear benchmark for strong selection. In reviewing many of the same studies as Kingsolver et al., Hereford et al. conclude that selection estimates are, on average, 54% as strong as selection on fitness (31% after correction for a statistical bias). In their view, these values represent "extremely strong selection overall" and "such large estimates clearly cannot be representative of selection on all traits"1. They then consider reasons for why current estimates of selection might be biased.

        These results1 raise some perplexing questions. Principal among them is the apparent paradox that typical studies of selection do not have the statistical power necessary (7, 8) to detect selection that appears unrealistically strong1. Unfortunately, this paradox will not be resolved simply by accumulating more data of the same ilk, as all reviews identify problems with our current methods (1, 4, 7, 8). How, then, are we to obtain a good handle on the true power of selection in nature?

        Evolutionary biologists will have to resolve this uncertainty by determining how best to measure and judge the strength of selection, and by conducting more robust studies of selection. Meanwhile, we are only deluding ourselves that we have a good handle on the typical power of selection in nature. Once we do, we can begin to investigate how humans are changing selection pressures, and whether populations and species will be able to adapt accordingly.

        References

1.  Hereford, J., Hansen, T. F. & Houle, D. Evolution 58, 2133-2143 (2004). | PubMed |
2. Darwin, C. On the Origin of Species (John Murray, London, 1859).
3.  Kettlewell, H. B. D. The Evolution of Melanism: The Study of a Recurring Necessity (Oxford Univ. Press, 1973). 
4. Endler, J. A. Natural Selection in the Wild (Princeton Univ. Press, 1986).
5.  Hendry, A. P. & Kinnison, M. T. Evolution 53, 1637-1653 (1999). | ISI |
6.  Stockwell, C. A., Hendry, A. P. & Kinnison, M. T. Trends Ecol. Evol. 18, 94-101 (2003). | Article | ISI |
7  Kingsolver, J. G. et al. Am. Nat. 157, 245-261 (2001). | Article | ISI |
8.  Hersch, E. I. & Phillips, P. C. Evolution 58, 479-485 (2004). | PubMed |
9. Grant, P. R. & Grant, B. R. Evolution 49, 241-251 (1995). | ISI |