I was mildly irritated to read a pamphlet in my doctor’s waiting room warning of the danger of failing to finish a course of antibiotic pills. Nothing wrong with that warning; but it was the reason given that worried me. The pamphlet explained that bacteria are ‘clever’; they ‘learn’ to cope with antibiotics. Presumably the authors thought the phenomenon of antibiotic resistance would be easier to grasp if they called it learning rather than natural selection. But to talk of bacteria being clever, and of learning, is downright confusing, and above all it doesn’t help the patient to make sense of the instruction to carry on taking the pills until they are finished. Any fool can see that it is not plausible to describe a bacterium as clever. Even if there were clever bacteria, why would stopping prematurely make any difference to the learning prowess of a clever bacterium? But as soon as you start thinking in terms of natural selection, it makes perfect sense.
Like any poison, antibiotics are likely to be dosage dependent. A sufficiently high dose will kill all the bacteria. A sufficiently low dose will kill none. An intermediate dose will kill some, but not all. If there is genetic variation among bacteria, such that some are more susceptible to the antibiotic than others, an intermediate dose will be tailor-made to select in favour of genes for resistance. When the doctor tells you to finish taking the pills, it is to increase the chances of killing all the bacteria and avoid leaving behind resistant, or semi-resistant, mutants. With hindsight we might say that if only we had all been better educated in Darwinian thinking, we would have woken up sooner to the dangers of resistant strains being selected. Pamphlets like the one in my doctor’s waiting room don’t help with that education – and what a sadly missed opportunity to teach something of the wondrous power of natural selection.
GUPPIES
My colleague Dr John Endler, recently moved from North America to the University of Exeter, told me the following marvellous – well, also depressing – story. He was travelling on a domestic flight in the United States, and the passenger in the next seat made conversation by asking him what he did. Endler replied that he was a professor of biology, doing research on wild guppy populations in Trinidad. The man became increasingly interested in the research and asked many questions. Intrigued by the elegance of the theory that seemed to underlie the experiments, he asked Endler what that theory was, and who originated it. Only then did Dr Endler drop what he correctly guessed would be his bombshell: ‘It’s called Darwin’s theory of evolution by natural selection!’ The man’s whole demeanour instantly changed. His face went red; abruptly, he turned away, refused to speak further and terminated what had hitherto been an amiable conversation. More than amiable, indeed: Dr Endler writes to me that the man had ‘asked some excellent questions before this, indicating that he was enthusiastically and intellectually following the argument. This is really tragic.’
The experiments that John Endler recounted to his closed-minded fellow passenger are elegant and simple, and they serve beautifully to illustrate the speed with which natural selection can go to work. It is fitting that I should use Endler’s own research here, because he is also the author of Natural Selection in the Wild, the leading book in which examples of such studies have been collected, and their methods laid out.
Guppies are popular freshwater aquarium fish. As with the pheasants we met in Chapter 3, the males are more brightly coloured than the females, and aquarists have bred them to become even brighter. Endler studied wild guppies (Poecilia reticulata) living in mountain streams in Trinidad, Tobago and Venezuela. He noticed that local populations were strikingly different from each other. In some populations the adult males were rainbow-coloured, almost as bright as those bred in aquarium tanks. He surmised that their ancestors had been selected for their bright colours by female guppies, in the same manner as cock pheasants are selected by hens. In other areas the males were much drabber, although they were still brighter than the females. Like the females, though less so, they were well camouflaged against the gravelly bottoms of the streams in which they live. Endler showed, by elegant quantitative comparisons between many locations in Venezuela and Trinidad, that the streams where the males were less bright were also the streams where predation was heavy. In streams with only weak predation, males were more brightly coloured, with larger, gaudier spots, and more of them: here the males were free to evolve bright colours to appeal to females. The pressure from females on males to evolve bright colours was there all the time, in all the various separate populations, whether the local predators were pushing in the other direction strongly or weakly. As ever, evolution finds a compromise between selection pressures. What was interesting about the guppies is that Endler could actually see how the compromise varied in different streams. But he did much better than that. He went on to do experiments.
Suppose you wanted to set up the ideal experiment to demonstrate the evolution of camouflage: what would you do? Camouflaged animals resemble the background on which they are seen. Could you set up an experiment in which animals actually evolve, before your very eyes, to resemble a background that you have experimentally provided for them? Preferably two backgrounds, with a different population on each? The aim is to do something like the selection of two lines of maize plants for high and low oil content that we saw in Chapter 3. But in these experiments the selection will be done not by humans but by predators and by female guppies. The only thing that will separate the two experimental lines is the different backgrounds that we shall supply.
Take some animals of a camouflaged species, perhaps a species of insect, and assign them randomly to different cages (or enclosures, or ponds, whatever is suitable) which have differently coloured, or differently patterned, backgrounds. For example, you might give half the enclosures a green foresty background and the other half a reddish-brown, deserty background. Having put your animals in their green or brown enclosures, you’d then leave them to live and breed for as many generations as you have time for, after which you’d come back to see whether they had evolved to resemble their backgrounds, green or brown respectively. Of course, you only expect this result if you put predators in the enclosure too. So, let’s put, say, a chameleon in. In all the enclosures? No, of course not. This is an experiment, remember; so you’d put a predator in half the green enclosures and half the red enclosures. The experiment would be to test the prediction that, in enclosures with a predator, the insects would evolve to become either green or brown – to become more similar to their background. But in the enclosures without a predator, they might if anything evolve to become more different from their background, to be conspicuous to females.
I have long nursed an ambition to do exactly this experiment with fruit flies (because their reproductive turnover time is so short) but, alas, I never got around to it. So I am especially delighted to say that this is exactly what John Endler did, not with insects but with guppies. Obviously he didn’t use chameleons for predators, but instead chose a fish called the pike cichlid (pronounced ‘sick lid’), Crenicichla alta, which is a dangerous predator of these guppies in the wild. Nor did he use green versus brown backgrounds – he opted for something more interesting than that. He noticed that guppies derive much of their camouflage from their spots, often quite large ones, whose patterning resembles the patterning of the gravelly bottoms of their native streams. Some streams have coarser, more pebbly gravel, others finer, more sandy gravel. Those were the two backgrounds he used, and you’ll agree that the camouflage he was seeking was subtler and more interesting than my green versus brown.
Endler got a large greenhouse, to simulate the tropical world of the guppies, and set up ten ponds inside it. He put gravel on the bottom of all ten ponds, but five of them had coarse, pebbly gravel and the other five had finer, sandy gravel. You can see where this is going. The prediction is that, when exposed to strong predation, the guppies on the two backgrounds will diverge from each other over evolutionary time, each in the direction of matching its own background. Where predation is weak or n
on-existent, the prediction is that the males should tend in the direction of becoming more conspicuous, to appeal to females.
Instead of putting predators in half the ponds and no predators in the other half, again Endler did something more subtle. He had three levels of predation. Two ponds (one fine and one coarse gravel) had no predators at all. Four ponds (two fine and two coarse gravel) had the dangerous pike cichlid. In the remaining four ponds, Endler introduced another species of fish, Rivulus hartii, which, despite its English name, ‘killifish’ (actually that’s quite irrelevant since it is named after a Mr Kille), is relatively harmless to guppies. It is a ‘weak predator’, whereas the pike cichlid is a strong predator. The ‘weak predator’ situation is a better control condition than no predators at all. This is because, as Endler explains, he was trying to simulate two natural conditions, and he knows of no natural streams that are totally free of predators: thus the comparison between strong and weak predation is a more natural comparison.
So, here’s the set-up: guppies were assigned randomly to ten ponds, five with coarse gravel and five with fine gravel. All ten colonies of guppies were allowed to breed freely for six months with no predators. At this point the experiment proper began. Endler put one ‘dangerous predator’ into each of two coarse gravel ponds and two fine gravel ponds. He put six ‘weak predators’ (six rather than one, to give a closer approximation to the relative densities of the two kinds of fish in the wild) into each of two coarse gravel ponds and two fine gravel ponds. And the remaining two ponds just carried on as before, with no predators at all.
After the experiment had been running for five months, Endler took a census of all the ponds, and counted and measured the spots on all the guppies in all the ponds. Nine months later, that is, after fourteen months in all, he took another census, counting and measuring in the same way. And what of the results? They were spectacular, even after so short a time. Endler used various measures of the fishes’ colour patterns, one of which was ‘spots per fish’. When the guppies were first put into their ponds, before the predators were introduced, there was a very large range of spot numbers, because the fish had been gathered from a wide variety of streams, of widely varying predator content. During the six months before any predators were introduced, the mean number of spots per fish shot up. Presumably this was in response to selection by females. Then, at the point when the predators were introduced, there was a dramatic change. In the four ponds that had the dangerous predator, the mean number of spots plummeted. The difference was fully apparent at the five-month census, and the number of spots had declined even further by the fourteen-month census. But in the two ponds with no predators, and the four ponds with weak predation, the number of spots continued to increase. It reached a plateau as early as the five-month census, and stayed high for the fourteen-month census. With respect to spot number, weak predation seems to be pretty much the same as no predation, over-ruled by sexual selection by females who prefer lots of spots.
So much for spot number. Spot size tells an equally interesting story. In the presence of predators, whether weak or strong, coarse gravel promoted relatively larger spots, while fine gravel favoured relatively smaller spots. This is easily interpreted as spot size mimicking stone size. Fascinatingly, however, in the ponds where there were no predators at all, Endler found exactly the reverse. Fine gravel favoured large spots on male guppies, and coarse gravel favoured small spots. They are more conspicuous if they do not mimic the stones on their respective backgrounds, and that is good for attracting females. Neat!
Yes, neat. But that was in the lab. Could Endler get similar results in the wild? Yes. He went to a natural stream that contained the dangerous pike cichlids, in which the male guppies were all relatively inconspicuous. He caught guppies of both sexes and transplanted them to a tributary of the same stream that contained no guppies and no dangerous predators, although the weak predator killifish were present. He left them there to get on with living and breeding, and went away. Twenty-three months later, he returned and re-examined the guppies to see what had happened. Amazingly, after less than two years, the males had shifted noticeably in the direction of being more brightly coloured – pulled by females, no doubt, and freed to go there by the absence of dangerous predators.
One of the nice things about science is that it is a public activity. Scientists publish their methods as well as their conclusions, which means that anybody else, anywhere in the world, can repeat their work. If they don’t get the same results, we want to know the reason why. Usually they don’t just repeat previous work but extend it: carry it further. John Endler’s brilliant research on guppies was just begging to be continued and extended. Among those who have taken it up is David Reznick of the University of California at Riverside.
Nine years after Endler sampled his experimental stream with such spectacular results, Reznick and his colleagues revisited the place and sampled the descendants of Endler’s experimental population yet again. The males were now very brightly coloured. The female-driven trend that Endler observed had continued, with a vengeance. And that wasn’t all. You remember the silver foxes of Chapter 3, and how artificial selection for one characteristic (tameness) pulled along in its wake a whole cluster of others: changes in breeding season, in ears, tail, coat colour and other things? Well, a similar thing happened with the guppies, under natural selection.
Reznick and Endler had already noticed that when you compare guppies in predator-infested streams with guppies in streams with only weak predation, colour differences are only the tip of the iceberg. There is a whole cluster of other differences. Guppies from low-predation streams reach sexual maturity later than those from high-predation streams, and they are larger when they reach adulthood; they produce litters of young less frequently; and their litters are smaller, with larger offspring. When Reznick examined the descendants of Endler’s guppies, his findings were almost too good to be true. The ones that had been freed to follow female-driven sexual selection rather than predator-driven selection for individual survival had not only become more brightly coloured: in all the other respects I have just listed, these fish had evolved the full cluster of other changes, to match those normally found in wild populations free from predators. The guppies matured at a later age than in predator-infested streams, they were larger, and they produced fewer and larger offspring. The balance had shifted towards the norm for predator-free pools, where sexual attractiveness takes priority. And it all happened staggeringly fast, by evolutionary standards. Later in the book we shall see that the evolutionary change witnessed by Endler and Reznick, driven purely by natural selection (strictly including sexual selection), raced ahead at a speed comparable to that achieved by artificial selection of domestic animals. It is a spectacular example of evolution before our very eyes.
One of the surprising things we have learned about evolution is that it can be both very fast – as we have seen in this chapter – and, under other circumstances, as we know from the fossil record, very slow. Slowest of all are those living creatures that we call ‘living fossils’. They are not literally brought back from the dead like Lenski’s frozen bacteria. But they are creatures that have changed so little since their remote ancestors that it is almost as though they were fossils.
Lingula
My favourite living fossil is the brachiopod Lingula. You don’t need to know what a brachiopod is. They would surely have been staples on the menu, had seafood restaurants flourished before the great Permian extinction a quarter of a billion years ago – the most catastrophic extinction of all time. A superficial glance might confuse them with bivalve molluscs – mussels and their kind – but they are really very different. Their two shells are top and bottom, where mussels’ shells are left and right. In evolutionary history bivalves and brachiopods were, as Stephen Jay Gould memorably put it, ships that pass in the night. A few brachiopods survived ‘the Great Dying’ (Gould’s phrase again), and modern Lingula (above) is so similar to Lingulella, th
e fossil below, that the fossil was originally given the same generic name, Lingula. This particular specimen of Lingulella goes back to the Ordovician era, 450 million years ago. But there are fossils, also originally named Lingula and now known as Lingulella, going back more than half a billion years to the Cambrian era. I should admit, however, that a fossilized shell is not a lot to go on, and some zoologists dispute Lingula’s claim to be an almost wholly unchanged ‘living fossil’.
Lingulella – almost identical to its modern relatives
Many of the problems that we meet in evolutionary argumentation arise only because animals are inconsiderate enough to evolve at different rates, and might even be inconsiderate enough not to evolve at all. If there were a law of nature dictating that quantity of evolutionary change must always be obligingly proportional to elapsed time, degree of resemblance would faithfully reflect closeness of cousinship. In the real world, however, we have to contend with evolutionary sprinters like birds, who leave their reptile origins standing in the Mesozoic dust – helped, in our perception of their uniqueness, by the happenstance that their neighbours in the evolutionary tree were all killed by a celestial catastrophe. At the other extreme, we have to contend with ‘living fossils’ like Lingula which, in extreme cases, have changed so little that they might almost interbreed with their remote ancestors, if only a matchmaking time-machine could procure them a date.
Lingula is not the only famous example of a living fossil. Others include Limulus, the horseshoe ‘crab’, and coelacanths, which we shall meet in the next chapter.