The Power of Natural Selection Sufficient Statistical Power to Detect Typical Andrew P

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Winterthurerstrasse 190, CH-8057 Zurich, 4. Karbowski, M. & Youle, R. J. Cell Death Differ. 10, 870–880 (2003). Burdened by the practical needs of gradua- Switzerland. 5. Frank, S. et al. Dev. Cell 1, 515–525 (2001). ting, I soon bowed out of the project and did e-mail: [email protected] 6. Kinchen, J. M. & Hengartner, M. O. Curr. Top. Dev. Biol. 65, not see the results until 2001. Surprisingly, it 1–45 (2004). seemed that Endler’s conclusions had swung 1. Jagasia, R., Grote, P.,Westermann, B. & Conradt, B. Nature 433, 7. Parrish, J. et al. Nature 412, 90–94 (2001). 754–760 (2005). 8. Horvitz, H. R. Cancer Res. 59, 1701s–1706s (1999). the pendulum too far back when Kingsolver 2. Danial, N. N. & Korsmeyer, S. J. Cell 116, 205–219 (2004). 9. Labrousse, A. M., Zappaterra, M. D., Rube, D. A. et al. emphasized that “directional selection 3. Hengartner, M. O. Nature 407, 770–776 (2000). & van der Bliek, A. M. Mol. Cell 4, 815–826 (1999). on most traits and in most systems is quite weak”7.This conclusion was largely based on the observation that most estimates of Evolutionary biology selection were non-significant and centred around zero. A particularly worrisome finding was that most studies did not have The power of natural selection sufficient statistical power to detect typical Andrew P. Hendry strengths of selection7,8.Perhaps the pendulum should swing all the way back to Darwin: Adaptation by natural selection is the centrepiece of biology. Yet natural selection really is weak in nature, evolutionary biologists may be deluding themselves if they think they except in exceptional situations. have a good handle on the typical strength of selection in nature. Enter Hereford et al.1,who argue that pre- vious reviews did not have objective criteria he one constant in our world is change of selection (Box 1).Endler’s review heralded by which to judge whether selection was — change often wrought by our own a shift in our perceptions when he empha- weak or strong. They suggest that this prob- Tdevices. In consequence, some of the sized that “strong selection is not rare and lem can be resolved if selection estimates for populations and species with which we may even be common”4, basing this conclu- individual traits are standardized to allow cohabit have difficulty persisting.Yet organ- sion largely on the observation that some comparison with the expected strength of isms should be able to adapt to changing studies documented quite strong selection. selection on fitness itself (Box 1). Selection environments, as they have done for billions Another way to infer the power of selec- on fitness,they argue,provides a clear bench- of years,diversifying into a bewildering array tion is to actually measure evolutionary mark for strong selection.In reviewing many of environments. But extinctions are also a changes in natural populations5,6.Studies of the same studies as Kingsolver et al.,Here- prominent feature of the past.Were these lost taking this approach often document sub- ford et al.conclude that selection estimates organisms unable to adapt to change? If so, stantial changes over short time intervals, are,on average,54% as strong as selection on are the rapid changes now being driven by suggesting that natural selection does indeed fitness (31% after correction for a statistical humans too much for adaptation to combat? have the power to drive rapid adaptation. bias). In their view, these values represent At the heart of these questions is the power of Darwin was too modest,it seemed,about the “extremely strong selection overall” and natural selection to bring about evolution- power of his idea. “such large estimates clearly cannot be repre- ary adaptation in natural populations. Fast-forward to 1998, when I joined a sentative of selection on all traits”1.They Writing in Evolution,Joe Hereford and discussion group led by Joel Kingsolver at then consider reasons for why current esti- colleagues1 bring this matter into stark relief. the University of Washington. This group mates of selection might be biased. The primary mechanism of adaptive set about analysing all studies of natural These results1 raise some perplexing evolution is natural selection, whereby org- selection published since Endler’s book. questions. Principal among them is the anisms possessing traits that improve their evolutionary ‘fitness’ — their survival and reproduction — contribute more genes to Box 1Measuring selection in natural populations subsequent generations. Yet perceptions of the power of selection have recently swung at On the small island of standardized strength of the end of a pendulum. Charles Darwin felt Daphne Major in the selection on beak depth that “natural selection will always act very Galapagos Islands, Peter and during the drought was A. P. HENDRY slowly, often only at long intervals of time, Rosemary Grant and S0.63 and 0.53. That is, and generally on only a very few of the inhab- colleagues9 measured the selection favoured large itants of the same region at the same time”2. beak size of all medium beaks because such beaks If Darwin was right,natural selection should ground finches (Geospiza could crack the harder seeds be almost imperceptible, and adaptation fortis, pictured) before a that remained. must require “the long lapse of ages”2.This drought. The abundance of Endler4 and Kingsolver perception held sway for more than a cen- seeds (particularly soft et al.7 compiled standardized tury before it was challenged by a series of seeds) decreased during the can be obtained by dividing S or values for many empirical studies — most famously those drought and finch mortality S by the variance for the studies and traits. Hereford showing dramatic changes in the coloration was high. When the drought trait ( can also be obtained and colleagues1 took a of peppered moths during industriali- ended but before from a regression of the trait similar approach, except that zation3.These studies inspired a wave of reproduction started, the on a measure of fitness, values were standardized interest in actually measuring selection and Grants determined the beak in this case survival). by the mean for the trait, adaptation in natural populations. size of all surviving finches. Selection estimates can be rather than its standard By the mid-1980s, enough studies had The difference in mean standardized by dividing S or deviation. Hereford et al. accumulated for John Endler to profitably beak size from before to after multiplying by the standard argue that the benefit of review them in his classic book Natural Selec- the drought is one measure deviation of the trait. is standardizing selection by tion in the Wild 4.Reviews of this sort typi- of the strength of selection additionally useful because it the mean is that the cally collate and combine selection estimates (S). A related measure is the can account for correlations corresponding value for for a variety of traits and studies so as to selection gradient, , which among traits. The fitness should be 1. A.P.H. address general questions about the strength

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apparent paradox that typical studies of investigate how humans are changing selec- selection do not have the statistical power tion pressures,and whether populations and necessary7,8 to detect selection that appears species will be able to adapt accordingly. ■ unrealistically strong1.Unfortunately, this Andrew P. Hendry is in the Redpath Museum and paradox will not be resolved simply by accu- Department of Biology, McGill University, mulating more data of the same ilk, as all Montreal, Quebec H3A 2K6, Canada. reviews identify problems with our current e-mail: [email protected] 1,4,7,8 methods .How, then, are we to obtain a 1. Hereford, J., Hansen, T. F. & Houle, D. Evolution 58, 2133–2143 100 YEARS AGO good handle on the true power of selection (2004). What mutation is in biology, conversion 2. Darwin, C. On the Origin of Species (John Murray, London, 1859). in nature? 3. Kettlewell, H.B.D.The Evolution of Melanism: The Study of a is in psychology, and revolution in sociology. Evolutionary biologists will have to Recurring Necessity (Oxford Univ. Press, 1973). It may be said that to assume such parallels resolve this uncertainty by determining how 4. Endler, J. A. Natural Selection in the Wild (Princeton Univ. Press, is merely to beg the question, but I think that best to measure and judge the strength of 1986). the apparent parallelism cannot be without 5. Hendry, A. P. & Kinnison, M. T. Evolution 53, 1637–1653 selection, and by conducting more robust (1999). significance… If the supposed analogy studies of selection. Meanwhile, we are 6. Stockwell, C. A., Hendry, A. P. & Kinnison, M. T. Trends Ecol. is a valid one, it appears to follow that only deluding ourselves that we have a Evol. 18, 94–101 (2003). mutability is due to the same general 7. Kingsolver, J. G. et al. Am. Nat. 157, 245–261 (2001). good handle on the typical power of selec- 8. Hersch, E. I. & Phillips, P. C. Evolution 58, 479–485 (2004). causes as ordinary variability (just as tion in nature. Once we do, we can begin to 9. Grant, P. R. & Grant, B. R. Evolution 49, 241–251 (1995). change of opinion and reform are due to the same general causes as conversion and revolution), but that there is this difference Planetary science — mutability represents an explosion of energy, as it were, in a given direction, and therefore differs from ordinary variation Saturn’s mixed magnetosphere somewhat as the firing of a gun differs Fran Bagenal from the explosion of a loose heap of powder… [T]he chance of mutations When interplanetary shock waves hit the Cassini spacecraft and then succeeding from the first is comparatively Saturn in January 2004, it presented a unique opportunity to study the remote, though such a thing is quite planet’s magnetosphere and to compare it with that of Earth. possible; but since they are the result of general causes, the sort of changes the aturn can be considered as the geo- Most of the material in Earth’s magneto- mutations exhibit are likely to come about metric mean of Earth and Jupiter in sphere is a plasma of protons and electrons in due course, just as the sort of changes Sterms of the strength and extent of its that has leaked in from the solar wind. By represented by a revolution are likely to magnetic field. Three papers in this issue — contrast, the magnetospheres of Jupiter and prevail ultimately, though the revolution by Clarke et al.1,Kurth et al.2 and Crary et al.3 Saturn are mainly fed by plasma sources of itself may appear to fail. T. D. A. Cockerell —describe the response of Saturn’s mag- heavy ions from their satellites. From Nature 16 February 1905. netosphere to changes in the solar wind as The three papers1–3,beginning on page observed by NASA’s Cassini spacecraft and 717, describe observations of magneto- 50 YEARS AGO the Hubble Space Telescope (HST). The sphere dynamics at Saturn. In Earth’s mag- Amazon Head-Hunters. By Lewis Cotlow. The authors conclude that some aspects of the netosphere, plasma circulates in a flow author of this book is a New York insurance behaviour of Saturn’s magnetosphere are pattern that is primarily driven by the cou- broker whose hobby is travelling in lands similar to the behaviour of Earth’s magneto- pling of the planetary magnetic field to the inhabited by primitive races… Between sphere,some to that of Jupiter’s and some are solar wind. Within about 15 of the poles, 1940 and 1949 he made several expeditions unique. Studies of Saturn’s magnetic field Earth’s magnetic field is directly connected to the north-west of the South American and how it is driven by the solar wind are to the solar wind.At lower latitudes the mag- continent… These are the areas inhabited interesting in their own right, but they also netic field topology is closed, with magnetic by the Choco, Colorado and Yagua Indians, allow researchers to compare different plan- field lines connected at both ends to the plan- and include also the very isolated country etary magnetospheres and to test our under- etary dynamo. At the outer boundary of the of the Jivaro Indians, who are especially standing of Earth’s system by applying the magnetosphere — the dayside ‘magne- known for their custom of drying and same principles to different conditions. topause’— small regions of closed magnetic shrinking the heads of their enemies… Earth’s magnetic field forms a cavity in field couple to the solar magnetic field Mr. Cotlow was able to become very the solar wind — the stream of electro- (which is swept towards the planet by the friendly with several of their chiefs, magnetic radiation and charged particles solar wind) in a process called magnetic and they informed him of the number of that flows outwards from the Sun. Earth’s reconnection. Once coupled to the solar heads which they had taken during their magnetosphere extends roughly 10 times the wind, these tubes of magnetic flux are swept lives. He brings out forcibly the fact that planet’s radius towards the Sun and many back over Earth’s poles and down the magne- the relatives of a man slain in battle are in hundreds of Earth radii away from the Sun, totail where they reconnect to closed field honour bound to kill his killer and to shrink in a ‘magnetotail’ stretching downstream lines — as they must, to conserve the total his decapitated head. The relatives of this of Earth in the solar wind. Jupiter is much magnetic flux from the planet. victim must retaliate in the same manner, larger than Earth (by a factor of 11), and The stresses associated with this process so that inter-community warfare is almost its magnetosphere is also vast, extending of coupling solar wind and magnetosphere continuous. The author describes fully the 50–100 jovian radii on the dayside, with a drive electrical currents between the mag- method of shrinking a head. Unfortunately, magnetotail that stretches out to its orbit netopause and the ionosphere (the ionized he did not actually see it carried out, since distance. Saturn’s magnetosphere (Fig. 1, upper part of the planet’s atmosphere), at the time of the raid he was stricken with overleaf) is an intermediate case, extending leading to radio and auroral emissions. The dysentery. about 20 Saturn radii towards the Sun terrestrial aurorae form in rings around From Nature 19 February 1955. (Saturn’s radius is 9.4 times that of Earth). Earth’s magnetic poles, at the boundaries