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with some scepticism, came from measure-ments made by the Ulysses spacecraft5. More recently, observations by the Cassini orbiter have confirmed that the period changes by as much as 1% or so in months to years6.

So, today, we know that the radio power is periodically modulated but we do not under-stand why. And we know that the radio period drifts too rapidly to be consistent with changes in the rotation period of the deep interior of a massive spinning planet. Other types of analy-sis give an estimate of the rotation rate of the deep interior that is distinctly shorter than the shortest period inferred from the radio clock7. Thus, it seems likely that the radio clock responds to processes in the planet’s upper atmosphere and magnetosphere. Explanations of the varying period of the radio clock have appealed to changing conditions that are either external to Saturn’s magnetosphere (such as the speed of the solar wind8) or internal to it (such as the mass injected from the vapour plume of Saturn’s small moon, Enceladus9). But evidence that such effects cause the observed drift in the period has been sketchy.

Zarka et al.1 use roughly three years of Cassini radio-wave data to provide compel-ling support for the hypothesis that external effects contribute to the modulation of the radio period. They find that the total power within a defined range of radio frequencies integrated over a full Saturn rotation period of 10.75 hours fluctuates on timescales of about 20–30 days. The properties of the solar wind are known to fluctuate at the solar rotation period of 25 days, and also to show trends over longer timescales. Zarka et al. find that cross-correlations with the speed of the solar wind are high, especially when Cassini’s co latitude (the difference between its latitude and 90°) remains relatively constant, relative to Saturn’s spin axis. The correlations with other properties of the solar wind (such as dynamic pressure) are weak.

Given evidence that the source of the radio emissions seems to be localized in the morning to noon sector8, it was previously proposed9 that changes in the period of the radio clock would occur if the source location shifts with changing solar-wind velocity. Such shifts could arise (and vary systematically with solar-wind velocity) if the emissions are triggered where the magnetospheric boundary becomes unstable through the growth of a phenom-enon known as Kelvin–Helmholtz waves (the equivalent for magnetized plasma of wave-breaking when high winds blow over water). This interpretation remains speculative: the new results do not establish a mechanism for the changing periodicity. But the knowledge that the radio period is modulated by the speed of the solar wind should help in the quest for a more complete understanding.

Many planetary scientists expected Saturn’s magnetosphere to be a bloated but rather boring analogue of Earth’s. The data being collected by Cassini continue to belie this

expectation. Ten years after its launch from Earth, the mission continues its fruitful explo-ration of a planetary system that is dramatically different from any previously investigated. ■

Margaret Galland Kivelson is at the Institute of Geophysics and Planetary Physics, University of California, Los Angeles, 6843 Slichter Hall, Los Angeles, California 90095-1567, USA. e-mail: mkivelson@igpp.ucla.edu

1. Zarka, P., Lamy, L., Cecconi, B., Prangé, R. & Rucker, H. O. Nature 450, 265–267 (2007).

FISHERIES

Nets versus natureDavid O. Conover

The life-histories of pike adjust quickly to shifts in the opposing forces of fishing and natural selection. Such rapid changes suggest that evolutionary dynamics must be incorporated into fisheries management.

People like to catch big fish, sometimes so much so that fish sizes overall become greatly diminished. According to one view, the contin-ual removal of large fish from a population sets the stage for rapid, undesirable evolutionary changes, including slower growth, earlier adult maturation and permanently smaller size1,2. This occurs because removing the largest fish directly opposes natural selection, which tends to favour large size.

What happens when these two forces simul-taneously oppose one another? Can evolution respond quickly enough to track changes in fishing selection, or does natural selection counteract it? Writing in Proceedings of the National Academy of Sciences3, Eric Edeline and colleagues illustrate the outcome of this dynamic tug-of-war between the forces of natural selection and fishing selection.

Until now, the theory underlying the management of fisheries has been based on ecological models that predict how the pro-ductivity of an exploited population changes in relation to its density, and the age and size at which fish are caught. The goal is to ensure a maximal but sustainable catch in perpetu-ity. Current management approaches do not take into account the potential for evolutionary change in response to fishing.

Why is evolution important to fisheries man-agement? It could be argued that fishing merely adds an additional predator to the ecosystem. But from the fish’s point of view, humans turn the rules of engagement completely upside down. Most natural predators attack smaller fish more frequently than larger fish. The bigger a fish gets, the lower its mortality (Fig. 1). Hence, growing fast early in life is a good strategy. Moreover, because big fish produce many more offspring than small fish, delaying maturation to larger size also

increases fitness — that is, the likelihood that one’s genes will be passed on to future genera-tions. By causing greatly increased mortality at large sizes, fishing selects for fish that grow slowly and mature at small sizes. Numerous other physiological, behavioural and repro-ductive traits likewise evolve that can lower fit-ness4. Taken to its extreme, many generations of intense size-selective fishing could in theory cause the evolution of a population of runts.

The introduction of darwinian principles into fisheries science has been controversial5,6. Some have argued that adequate proof of evolu-tionary changes caused by fishing has not been demonstrated. That would require changes in traits such as growth rate to be shown to have a genetic basis. This is extremely difficult to do

Figure 1 | The darwinian struggle between natural selection and fishing selection. The graph depicts the contrast between mortality rates as a function of fish size in the absence and presence of mortality due to fishing. Natural rates of mortality decline dramatically with increasing size early in life, until reaching a low level for the remainder of life (purple). Fishing greatly increases the mortality of large fish (green). Arrows represent the direction of selection on body size in the absence (purple arrow) and presence of fishing (green arrow).

2. Riddle, A. C. & Warwick, J. W. Icarus 27, 457–459 (1976).3. Desch, M. D. & Kaiser, M. L. Geophys. Res. Lett. 8, 253–256

(1981).4. Giampieri, G., Dougherty, M. K., Smith, E. J. & Russell, C. T.

Nature 441, 62–64 (2006).5. Galopeau, P. H. M. & Lecacheux, A. J. Geophys. Res. 105,

13089–13102 (2000).6. Gurnett, D. A. et al. Science 316, 442–445 (2007). 7. Anderson, J. D. & Schubert, G. Science 317, 1384–1387

(2007).8. Galopeau, P. H. M., Zarka, P. & Le Quéau, D. J. Geophys. Res.

100, 26397–26410 (1995).9. Cecconi, B. & Zarka, P. J. Geophys. Res. 110, A12203,

doi:10.1029/2005JA011085 (2005).

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in the wild because environmental and genetic influences are confounded, although new statistical methods have enabled the evolution of certain traits (such as size at maturity) to be revealed7. Lab experiments, in which envi-ronmental conditions are standardized, can demonstrate genetic change8 but have been criticized for not representing real fisheries in the wild5.

Edeline et al.3 now enter the fray. They took advantage of a unique 50-year time series of data on growth rates of pike (Esox lucius) in Lake Windermere in northwest Eng-land. This lake was fished for centuries until 1921, when the net fisheries were closed. Net fishing did not reopen until 1944. Each year from 1944 onwards, biologists tracked the age and growth of individual pike landed in the fishery by measuring the annual rings that form in certain bones, much like reading the rings in a tree trunk. They also tagged and recaptured pike, providing estimates of population size and mortality.

These highly detailed data enabled the authors to show in an earlier paper9 that fish-ing did indeed remove the larger, faster-grow-ing fish whereas natural sources of mortality did the opposite. Hence, they hypothesized that the sudden resurgence of fishing in 1944 should cause an evolutionary decline in growth rate followed later by an increase as the fishery waned over the 50 years. After using statisti-cal models to account for the effect of a suite of confounding environmental factors, the temporal trend in growth rate closely tracked the predicted pattern. Several twists and turns in growth trajectory seemed to coincide with episodes of excessively high fishing and with the large-scale death of perch (a prime food source for pike) in 1976. In addition, changes occurred in the level of reproductive invest-ment by young females that were also as pre-dicted from evolutionary theory. The authors conclude that evolutionary responses to the opposing forces of fishing and natural selection must be accounted for in managing fisheries.

Critics will contend that consistency with the predictions of evolution is not proof that the changes observed were in fact genetic. The responses are probably far too rapid to be entirely evolutionary as opposed to ecological in origin. With only one population under study, any interpretation of this sequence of growth changes contains an element of story-tell-ing. Perhaps the changes in growth rate fit the predictions of evolution purely by coincidence.

Yet this is one of the most data-rich and comprehensive analyses of fishery-induced evolution ever published. Together with strong evidence also emerging from a variety of other harvested species7,10–12, the likelihood that all such studies are erroneous is becoming vanish-ingly small. Moreover, Edeline and colleagues’ approach provides fresh incentive and the methodology to test for evolutionary change in the many other long-term data sets of age and growth that exist for heavily fished species. ■

David O. Conover is in the School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York 11794-5000, USA.e-mail: dconover@notes.cc.sunysb.edu

1. Law, R. ICES J. Mar. Sci. 57, 659–668 (2000).2. Stokes, T. K., McGlade, J. M. & Law, R. The Exploitation

of Evolving Resources (Springer, Berlin, 1993).3. Edeline, E. et al. Proc. Natl Acad. Sci. USA 104, 15799–15804

(2007).4. Walsh, M. R., Munch, S. B., Chiba, S. & Conover, D. O.

DEVELOPMENTAL BIOLOGY

The power of blood Paige Snider and Simon J. Conway

Compared with the masterpiece crafted by nature, even Leonardo da Vinci’s anatomical drawings of the cardiovascular system seem primitive. In creating this system, nature seems to use blood flow as its paintbrush.

More than a century ago, Thoma noted1 that blood vessels carrying a high volume enlarge, whereas those with low flow regress. Since then, significant evidence has accumulated to sug-gest that the mechanical force created by blood flow affects gene expression in the developing embryo2,3. But how does blood flow contribute to shaping a functional vascular architecture, when vessel identity and developmental pat-terning are genetically predetermined? On page 285 of this issue, Yashiro et al.4 take a step towards solving this puzzle by showing that an interplay between haemodynamics (the dynamics of blood flow) and genetic factors mediates cardiovascular development.

Among the most common congenital birth defects are abnormalities in the growth and development of the cardiovascular system; in particular, anomalies in the asymmetric remod-elling of a transient structure known as the branchial arch artery apparatus that occurs in 6–7-week-old human embryos5. Mammals have five branchial arches, each of which contains an arch artery (numbered 1–4 and 6). Blood flows out of the heart via branchial arch arteries to circulate throughout the embryo. Although the arterial system initially forms symmetrically (Fig. 1a), in the mature organism, the left fourth and sixth arch arteries persist and give rise to the aortic arch and pulmonary trunk, whereas the right fourth and sixth arch arteries regress (Fig. 1b). This results in the asymmetric develop-ment of the great vessels of the ventricular outflow tract5, which forms part of the left and right ventricles.

A likely candidate for directing asymmetric development was the transcription factor Pitx2, which is the product of the only gene known to be asymmetrically expressed in the embry-onic tissue that generates the branchial arch6–9. Moreover, Pitx2 is induced by Nodal, a signal-ling molecule that regulates the initial establish-ment of left–right patterning in the embryo6.

But the overall mechanisms — or genetic path-ways — that govern asymmetric development of the artery arches remained elusive.

In search of an answer, Yashiro et al.4 used mutant mice that do not express physiologi-cally significant levels of Pitx2 in the left side of their ventricular outflow tract. The authors found that this mutation prevents normal rota-tional movement of the outflow tract, which is essential for remodelling of the right sixth arch artery into a long, narrow vessel with reduced blood flow. Consequently, they observed that in about half of the mutant mice the right sixth arch artery persists in its initial morphology.

This finding led Yashiro and colleagues to propose that, in normal mice, reduced blood flow through the right sixth arch artery leads to its regression. To test this hypothesis, they per-formed a clever microsurgical procedure to ‘tie off ’ the left sixth arch artery, thereby reducing blood flow through it (Fig. 1c). They reasoned that if this treatment causes un expected regres-sion of the left sixth arch artery, then haemo-dynamics has a pivotal role in the asymmetric development of the arterial system. They found that microsurgical ligation of this artery does result in its regression, and that the usually regressing right sixth arch artery — which after ligation receives normal levels of blood — persists.

The authors went on to show that another factor that contributes to normal arch-artery remodelling is the asymmetric expression of vascular growth factors such as PDGF and VEGF, because inhibition of these factors results in the loss of both the left and right sixth arch arteries. Remarkably, they find that only the sixth arch arteries are sensitive to growth-factor-mediated signalling pathways, as the remodel-ling of the fourth arch artery was not affected by inhibition of these factors’ receptors.

Although sixth arch arteries depend on Pitx2 for their normal, asymmetrical remodelling9,

Ecol. Lett. 9, 142–148 (2006).5. Hilborn, R. Fisheries 31, 554–555 (2006).6. Conover, D. O. & Munch, S. B. Fisheries 32, 90–91 (2007).7. Olsen, E. M. et al. Nature 428, 932–935 (2004). 8. Conover, D. O. & Munch, S. B. Science 297, 94–96

(2002).9. Carlson, S. M. et al. Ecol. Lett. 10, 512–521 (2007).10. Haugen, T. O. & Vøllestad, L. A. Genetica 112–113, 475–491

(2001). 11. Swain, D. P., Sinclair, A. F. & Hanson, J. M. Proc. R. Soc.

Lond. B 274, 1015–1022 (2007). 12. Coltman, D. W. et al. Nature 426, 655–658 (2003).

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