Box 2.3 Quantitative trait locus (QTL) analysis
2.4.2 Responses to selection
Is there any evidence that variation in behaviour responds to selection? We shall look at two lines of evidence that suggest it does: the response of behavioural traits to artificial selection, and heritable differences in behaviour associated with presumed differences in selection pressure in the natural environment.
2.4.2.1 Responses to artificial selection
Artificial selection usually involves taking a genetically variable population, testing indi-viduals for the behavioural characteristic of interest, say aggressiveness or learning speed, then pairing high-scoring males with high-scoring females and vice versa to create opposing selected lines. The procedure is repeated over a number of generations to see whether the average score of the population increases or decreases accordingly (see Fig. 2.5b). It is also good practice to create a third line of randomly mated pairs to monitor any underlying drift in the selected character over the period of the experiment.
Such experiments rarely fail to show changes in the selected direction, implying that much of the continuous variation in behaviour within populations is genetic and able to respond to selection. Some examples are shown in Fig. 2.11.
Of course, many of the behaviours selected for or against in these kinds of experi-ment are complex characters that are the end product of many underlying processes, quite possibly different in different individuals. High learning ability, for example, may reflect good memory, attentiveness, boldness in exploration or a number of other attributes. An initial trawl of good learners and poor learners from a starting population could include any or all of these causes, and it can be instructive to see what is selected 2.4 n Natural selection and ‘selfish genes‘ x 57
Figure 2.10 Some typical sexually selected characters. (a) Antlers in many large herbivorous mammals are used by males to fight for access to females, while various mate-guarding behaviours, such as that of the freshwater shrimp Gammarus pulex (b), are designed to reduce post-copulatory competition from the sperm of rival males. Elaborate adornments, such as the long tail of male birds of paradise (c) are generally assumed to have evolved through female choice. See text and Chapter 10. After Gould & Gould (1989) and Krebs & Davies (1993).
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along with the trait of interest as the selection process proceeds. A nice example comes from a study of tameness in silver foxes (Vulpes vulpes) by Dmitry Belyaev (1979).
Belyaev was interested in the evolution of domestication in dogs. As predators and scavengers, often hunting in packs, dogs are not the most obvious candidates for companionship with humans, and indeed the behaviour of wild dogs towards people is vastly different from that of the familiar domestic animal. The word we use to sum up the difference is ‘tameness’. Generally, the tamer an animal the less likely it is to attack us or run off, and the more likely it is to appear friendly. But these are complex traits, and only a handful of those we might want to incorporate into our estimate of tameness in any particular case (Price 2002). So what does constitute tameness and what changes as tameness evolves? To find out, Belyaev conducted an artificial selection experiment with his foxes.
Figure 2.11 Some examples of artificial selection for behavioural attributes. (a) Results of selection for increased (solid lines) and reduced (dotted lines) open field activity (locomotory activity in an open arena) in laboratory mice. The dashed lines are randomly mated controls. After DeFries et al. (1974).
Silver foxes are close enough to the domestic dog’s jackal ancestor to provide a reasonable starting point for a selection experiment. They are also bred commercially for their fur, so were readily available for Belyaev’s experiment. Belyaev’s first problem, however, was to decide what to select. Since tameness is a complex character, his approach was to select on the basis of a broad range of aggressive, fearful, friendly and inquisitive responses towards the experimenters. He then selectively mated the tamest foxes by these criteria each generation and continued until the process had been carried out for 18 generations. Figure 2.12 summarises the outcome. The x-axis in the figure represents Belyaev’s composite ‘tameness’ score, with tameness increasing to the right and decreasing to the left. As the generations go by, the distribution of the tameness score shifts to the right, from the aggressive end of the scale in the original, unselected population towards tamer values by generation 18. Thus variation in tameness among the foxes had a genetic basis and responded to selection. What was especially interesting, however, was that, along with the behavioural characteristics actively selected by Belyaev, came a range of other behaviours which echoed those of domestic dogs, for example approaching people and licking their hands and faces, or barking and tail-wagging when a person came into view. How did these associated changes come about?
As well as tracking changes in behaviour in his fox populations, Belyaev also measured changes in various hormones, among them serotonin, which is known to inhibit certain kinds of aggression and play an important role in the central regulation of stress and sex hormone secretion. When he compared hormone levels in his selected and unselected 2.4 n Natural selection and ‘selfish genes‘ x 59
Figure 2.11 (continued) (b) Selection for migratory tendency in blackcaps (Sylvia atricapilla).
Starting from a parental population in which about 75% of birds migrate, lines of non-migrators could be produced in six generations of selection, and lines of 100% migrators in three. Numbers indicate how many birds were reared in each generation. Note the reversed scaling of the y-axis.
Reprinted with permission after ‘Genetic basis of migratory behavior in European warblers’, Science, Vol. 212, pp. 77–9 (Berthold, P. and Querner, U. 1981). Copyright 1981 American Association for the Advancement of Science.
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lines, Belyaev found higher concentrations of serotonin and (in females over the first few days of pregnancy) the reproductive hormones oestradiol and progesterone in animals that had been selected for tameness He also found reduced levels of corticosteroids and associated changes in adrenal gland morphology in his tame foxes. Selection for tame-ness therefore appeared to be associated with changes in hormones associated with the neuroendocrine control of metabolism and development. Thus what Belyaev may have Figure 2.12 The distribution of ‘tameness’
scores in silver foxes after different genera-tions of artificial selection. Modified from Belyaev (1979).
done by using his composite behavioural selection criterion was actually select for changes in the mechanisms regulating early ontogeny. Since these affected a wider range of behaviours than those chosen by Belyaev, the additional tameness characteristics were incidentally affected too. These changes in physiological profile were also accompanied by changes in the reproductive cycle (towards two oestrous cycles a year [dioestrousness]) and external appearance (drooping ears, turned-up tails and variegated coat colours began to appear, for example) towards features familiar in domestic dog breeds. The experiment thus illustrates nicely what we stressed at the beginning of this chapter:
behaviour patterns evolve in concert with their underlying mechanisms. Function and mechanism are two sides of the same coin.
2.4.2.2 Adaptive differences between species populations
If selection has shaped behaviour in response to the demands of the local environment, then changes in environmental selection pressures should result in different adaptive behaviours. Populations of a given species living in different environments should thus show appropriate differences in behaviour. Several studies suggest this is the case. Prey choice in gartersnakes (Thamnophis elegans) is a good example.
Slugs and gartersnakes
Arnold (1980, 1981) studied gartersnakes from two regions of California: the low, wet, coastal region and the drier interior uplands. Coastal and inland snakes differed markedly in their diets. Coastal snakes, hunting in a warm, humid environment, took mainly slugs, while inland snakes, coming from a dry environment that did not support slugs, took mainly fish and frogs, which they caught in lakes and streams. The interesting question, however, is whether inland snakes would take slugs if given the opportunity. When Arnold offered slugs to wild-caught inland snakes he found they refused to eat them.
However, this may not be very informative, because their prior experience of fish and frogs may cause wild-caught snakes to reject slugs simply because they are novel. Arnold therefore used isolated captive-born snakes from the two regions to eliminate any effects of different feeding experience or social influence. Once again, he found that most inland snakes refused to take slugs, while coastal snakes took them quite happily (Fig. 2.13).
Arnold then went a stage further and tested the response of isolated newborn snakes that had never fed on anything to the odour of slugs presented on a cottonwool swab.
He counted the number of tongue flicks directed by snakes from the two environments at swabs soaked in different prey fluids. While there was a greater spread of response this time, there was still a marked difference in the acceptability of slug extract between inland and coastal snakes. By comparing the tongue flick rate of siblings within each population, Arnold was able to determine the percentage variation in response that was due to genetic as opposed to environmental differences between them. It turned out that only about 17% of the difference in response had a genetic basis, implying that genetic variation in responsiveness to slug odour had all but disappeared in the two populations.
Thus most coastal snakes have the allele(s) that allow them to detect and respond to slug odour, while most of the inland population have different alleles that do not. Crossing snakes from the two populations produced a variety of responses (see Box 2.2), but most individuals refused to take slugs. The difference in slug acceptance between the populations thus has a strong genetic basis with the allele(s) for slug rejection being dominant to that (those) for acceptance.
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But why has this happened? While it is easy to envisage a selective advantage to taking slugs where they are an abundant source of food, as they are on the coast, it is not obvious why snakes should reject slugs if they live inland. The answer seems to be to avoid ingesting leeches. Arnold has shown that the tendency to accept slugs predisposes snakes to accept leeches. Eating leeches is a bad idea because they can live on in the gut and potentially cause serious damage. This is not a problem along the coast because there are no leeches. Inland, however, they abound in the lakes in which the snakes hunt. A taste for soft, mucus-laden invertebrates here could prove fatal.
Temperature and rhythmicity in fruit flies
A different example comes from a geographical survey of the period gene in Drosophila (see 2.3.2.1). Costa et al. (1992) looked at geographical variation in the protein encoded by the period gene in D. melanogaster. The protein is characterised by an alternat-ing series of threonine–glycine (amino acid) pairs, and the region of the gene encodalternat-ing the repeat varies in length across populations of D. melanogaster. Costa et al. sampled populations from 18 locations across Europe and North Africa and looked at the frequency of different threonine–glycine alleles at each one. What they found was a marked latitudinal trend (a north–south cline) in the frequency of some of the alleles (Fig. 2.14). Why should this be?
A clue came from some genetic transformation experiments in which the efficacy of inducing arrhythmia using a perotransformation (see 2.3.2.1) with the threonine–glycine element removed was affected by temperature. Recovery of the arrhythmic phenotype was good at 25 °C but much weaker at 29 °C. The threonine–glycine repeat therefore appeared to be important for the thermal stability of the circadian rhythm. Subsequent behavioural experiments have convincingly confirmed this (Sawyer et al. 1997). Under different temperature regimes, the periodicity of the clock differs subtly between the major threonine–glycine variants, with the common southern variant (17 repeats) having Figure 2.13 The distribution of responses to cubes of slug by naïve laboratory-reared garter-snakes from inland and coastal populations in California. Snakes derived from coastal populations showed high feeding scores, while those from inland populations generally refused to feed. From Alcock (1998) after Arnold (1980).
a period close to 24 hours under hotter conditions, and the most abundant northern variant (20 repeats) having a period that is better buffered against temperature swings (i.e. is better temperature compensated) (Costa & Kyriacou 1998). Each variant is thus adapted to its particular climatic environment. Furthermore, studies of the molecular conformation of the region have shown that the variants predominating in natural popula-tions (14, 17, 20 and 23) have significantly better responses to temperature perturbapopula-tions than other variants (e.g. 15 and 21) (Sawyer et al. 1997; Fig. 2.14b). The significance of the north–south cline thus appears to be that different threonine–glycine alleles confer different adaptive circadian responses to geographical variation in temperature.