编者按：候鸟对不同气候的选择和适应性，不仅仅是长期的适应结果，也是由基因决定的。
Nature 425, 779 - 780 (23 October 2003); doi:10.1038/425779a
Metabolism: It's in the genes
ROBERT W. FURNESS
Robert W. Furness is at the Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, UK.
e-mail: r.furness@bio.gla.ac.uk
Warm-blooded animals of the same species, living in different climates, have different metabolic rates. In birds, this variation is not only due to physiological adaptation — it is inherent in the animals' genes.
Reptiles tend to live in warmer parts of the world because their low metabolic rate hinders life in cold climates. Birds and mammals, on the other hand, have high metabolic rates, which allow them to exploit colder climates by maintaining their body temperatures far above ambient conditions. But many species of bird and mammal are found in both cold and warm climates and metabolism can vary between the different populations. Are these variations driven by physiological adaptations to the local climate, or are they hard-wired into the animals' genetic make-up? Writing in the Proceedings of the Royal Society, Wikelski et al.1 suggest that the metabolic rate of birds is a genetically determined characteristic that can respond to selection pressures inherent in the different regions in which the birds live.
The gross differences in metabolic rate between cold-blooded reptiles and warm-blooded birds and mammals are well known, but the patterns of variation between closely related species, or indeed within individual species, are less well understood. Wikelski and colleagues1 have now examined the variation in the metabolic rates of different populations of a single species of bird. The authors made an outstanding choice of study species. They needed a species that could be reared in captivity easily, and that existed as several genetically distinct populations, inhabiting a wide range of climates. They chose to work with stonechats (Saxicola torquata; Fig. 1), a species of bird with several widely distributed 'races'. They show that stonechats from a tropical climate with little seasonal variation (Kenya) have a consistently low metabolic rate, whereas birds from a cooler but still fairly mild climate (Ireland) have a somewhat higher metabolic rate. And birds from colder climates (Austria and Kazakstan) have by far the highest metabolic rates.
Figure 1 A little bird with a lot of variation. Full legend
High resolution image and legend (99k)
It was demonstrated several years ago that metabolic rate increases with latitude2, 3 (a rough proxy for cold climate), but the crucial aspect of Wikelski and colleagues' study is that, from a very early age, all the birds were reared in captivity under the same conditions. So the variations between birds from the different populations could not be due to physiological adaptations to their respective local climates. Instead, the authors suggest that the differences in metabolic rate are specified by their genes.
What selective pressures shape the genetic make-up of different stonechat populations? Stonechats living in mild climates are year-round residents, whereas in locations with harsh winter climates, the birds are long-distance migrants. So the higher metabolic rate of stonechats from the Austrian and Kazakstan populations could be a consequence of selective pressures associated with migration. Wikelski et al. suggest that this is not the case because, energetically, migration is a cheap option compared with thermoregulation. The high metabolic rates of the Austrian and Kazakstan populations are more likely to be selected for by occasional periods of freezing temperatures during the breeding season.
Survival of warm-blooded animals in cold climates is possible only if food consumption is sufficient to meet the energy requirements for maintaining body temperature. But high metabolism has other costs besides increasing appetite — lifespan correlates inversely with heart rate across a wide range of mammal species. Mammals with low metabolic rates (and therefore slow heart rates) tend to live longer. Indeed, the relationship between metabolic rate and senescence is a central issue in the study of longevity4. Higher metabolic rates lead to faster cell divisions and a more rapid accumulation of mutations, which might eventually impair cell function and contribute to the ageing process. So the lower metabolism of Kenyan stonechats will allow them to survive better where food is scarce, and might also permit slower senescence. This indeed appears to be a general feature of tropical birds and mammals: the pace of life is slow, but survival is high.
Wikelski and colleagues have looked at how metabolic rate varied between populations, but other researchers have investigated the variation within single populations. In these studies, between half and two-thirds of the inter-population variation was attributed to individual characteristics that remained unchanged in individuals from year to year5. So these studies also hint at a genetic basis for metabolic rate. And seasonal6 or between-individual7 variations in organ size and other aspects of body composition explained much of the individual variation. It seems that the selective pressures that influence metabolism may be complex, influencing metabolic rate through affecting the density of mitochondria — the energy-producing organelles inside cells — or the size of the muscles or liver.
The genetic basis of metabolic rate has far-reaching implications. For example, it is now apparent that metabolism should be considered when selecting animal populations to reintroduce into particular environments. Recent reintroduction programmes brought Scandinavian red kites to Scotland but Iberian kites to England. Which is the better source population? If Scandinavian kites have a higher metabolic rate than their Iberian relatives, they will be better adapted to surviving cold conditions, but they will need more food to sustain them.
The new study1 raises many other questions. Have island populations evolved lower metabolic rates to cope with food scarcity? Have equivalent selection pressures shaped other features, such as insulating plumage or pelt, to match the variations in metabolism? Within a population, do individuals with lower metabolic rates have a slower pace of life? Wikelski et al. have demonstrated that metabolic rate is a genetic characteristic that can respond to selective pressure. But, as these questions show, there is a lot more to learn about how the environment shapes the evolution of this characteristic.
References 1. Wikelski, M. et al. Proc. R. Soc. Lond. B doi:10.1098/rspb.2003.2500 (2003). | PubMed |
2. Klaassen, M. Oecologia 104, 424-432 (1995). | ISI |
3. Bryant, D. M. & Furness, R. W. Ibis 137, 219-226 (1995). | ISI |
4. Kirkwood, T. B. L. Nature 270, 301-304 (1997).
5. Bech, C., Langseth, I. & Gabrielsen, G. W. Proc. R. Soc. Lond. B 266, 2161-2167 (1999). | Article | ISI |
6. Bech, C. et al. Comp. Biochem. Physiol. A 133, 765-770 (2002). | Article | ISI | ChemPort |
7. Bech, C. & Ostnes, J. E. J. Comp. Physiol. B 169, 263-270 (1999). | Article | ISI |
