Differences between strains
Genetic strains within species usually differ at many loci and provide a wealth of evidence for a genetic basis to different behaviour patterns. The genetic ‘purity’ of strains depends on the level at which they are defined. Thus strains in terms of different populations of the same species will differ more widely in their genotypes than those derived from controlled laboratory breeding programmes. Because of this, most work has been done with inbred laboratory strains. Serial inbreeding increases homozygosity and thus genetic uniformity within lines, but also, because the particular alleles that go to fixation at any given locus is a matter of chance, differences between lines. Extensive work with laboratory mice have shown differences between strains in, among other things, aggressiveness (Southwick 1968), mating behaviour (McGill 1970) and maze learning (Upchurch & Wehner 1988; Rousse et al.
1997), as well as various behavioural pathologies such as audiogenic seizure (seizures induced by loud sound; Fuller & Thompson 1978). Such differences are evident even when post- and prenatal experience is accounted for (e.g. by cross-fostering [Southwick 1968] or ovarian transplant [DeFries et al. 1967; Robertoux & Carlier 1988]). Local population-level strains among various invertebrates have similarly revealed differences in, e.g., mating behaviour (the mosquito Aedes atropalus; Gwadz 1970) and foraging communication (honey bees, Apis mellifera; Dyer & Seeley 1991).
Effects of chromosomal changes
Differences in behaviour can sometimes be traced to chromosomal abnormalities. Many of these are deleterious and, if not lethal, give rise to grossly dysfunctional phenotypes.
Abnormalities take three basic forms: (a) a change in the entire complement of chromosomes (euploidy) from, say, diploid (2n) to haploid (n) or triploid (3n) (multiplication of the complement is known as polyploidy), (b) the addition or loss of a single chromosome (aneuploidy) and (c) chromosome breakage. Evidence for relationships between polyploid events and behaviour is thin, but there are suggestive associations with dietary preferences in diploid and triploid whiptail lizards (Cnemidophorus tesselatus) (Paulissen et al. 1993) and call structure in poly-ploid tree frogs (Hyla versicolor) (Keller & Gerhardt 2001). In contrast, aneupoly-ploid changes are associated with a wide range of behavioural effects, mostly pathological, such as the cognitive, motor and sexual retardation accompanying an extra copy of chromosome 21 ( Trisomy 21 or Down’s syndrome) in humans and chimpanzees (Pan troglodytes), and the personality and spatial orientation problems associated with changes in the complement of sex chromosomes (e.g. Turner’s and Klinefelter’s syndromes). Changes through chromosome breakage can occur in four ways (Fig. (i)). Inversions are of some significance because the reversal of genetic material prevents normal crossing over during meiosis so that inverted sequences are transmitted as single units (linkage groups). Inversion karyotypes appear to be main-tained in various natural populations of flies through their effects on mating speed (Brncic &
Koref-Santibañez 1964; Speiss & Langer 1964, 1966; Crean et al. 2000).
Hybridisation and polygenic traits
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Ehrman & Parsons (1981). But while approaches such as those in Box 2.2 can tell us that many genes underlie behaviour, they do not tell us how many genes are involved or where they are on the animal’s chromosomes. Some steps towards this have been made by so-called cosegregation studies, in which the pattern of segregation of behaviours and genetic markers yield some clues as to the loci influencing behaviour (e.g. Hunt et al. 1995), but recent developments in molecular genetic techniques may now allow us to say much more.
Box 2.2 continued
Figure (i) The four major changes in gene sequence arising from chromosome breakage: dele-tion, duplicadele-tion, inversion and translocation. After Ehrman & Parsons (1981).
rearrangement of one particular gene. In principle, a single gene difference could also underlie a behavioural difference between inbred strains. Other evidence, however, demon-strates very clearly that many behaviours are under the influence of several different loci (i.e. are polygenic). Hybridisation is one approach that has been used widely to look at such traits. When two closely related species with different forms of a particular behaviour are crossed, the pattern of segregation of the behaviour in the resulting offspring tells us some-thing about the number of loci influencing it. In Dilger’s (1962) classic study of nest-building in lovebirds (Agapornis spp.), for example, hybrid crosses between peach-faced (A. roseicollis) and Fischer’s (A. fischeri ) lovebirds yielded offspring with a variety of (usually dysfunctional) combinations of nest-building behaviours characteristic of the two parental species, implying that nest-building in the two species was controlled by several independently segregating loci. The same was true for other behaviours in the birds, such as courtship (Dilger 1962).
Crosses between inbred strains of mice have shown that various strain differences in behaviour have similarly scrambled patterns of inheritance, again implying polygenic control (see Ehrman & Parsons 1981).
Quantitative trait loci
Quantitative trait locus (QTL) analysis, developed in its present form in the late 1980s, is one of a number of techniques that allows us to trace the different genes, or at least their position on particular chromosomes, underlying polygenic traits. QTL analysis can be done on any species for which there are inbred strains. The basic procedure is summarised, using maze-learning in mice as a hypothetical example, in Box 2.3. The process uses cross-breeding between strains and strain-specific genetic markers to seek associations between genotype at particular points along an organism’s chromosomes and the possession of a given phenotypic trait. QTLs emerge as a series of locations, often on several chromosomes, that contribute to the trait. Several behavioural traits have been traced to particular chromosomal positions using the approach. Fear conditioning is one example.
Inbred strains of mice differ in their tendency to show conditioned (trained to be expressed in response to particular stimuli; see Chapter 6) fear, suggesting a degree of genetic influence. Wehner and colleagues have looked at differences in fear responses under different contextual and stimulus conditions in a number of inbred strains. In BXD recombinant mice, correlations between strain genetic markers and conditioning responses suggested multiple QTLs. The strongest associations were on chromosomes 1 and 17, for freezing to context. However, associations also emerged on chromosome 12 for freezing to an altered context, and again on chromosome 1 for responses to an auditory stimulus (Owen et al. 1997). Using C57BL/6J and DBA /2J mice, QTLs for contextual conditioning mapped to chromosomes 10 and 16, with further suggestive sites on chromosomes 1, 2 and 3 (Wehner et al. 1997).
Tafti et al. (1997) traced QTLs associated with patterns of sleep in CXB recombinant mice. Sleep during the light period was associated with loci on chromosome 7, while that in the dark period mapped to chromosome 5, near the locus controlling activity cycles (the mouse equivalent of the period gene in Drosophila [see above]). The periodicity of sleep was influenced by yet other sites on chromosomes 2, 17 and 19.
More recently, QTL analysis has been used in Drosophila itself, and has indicated a large phenotypic effect of three chromosomal locations on courtship song (Gleason et al. 2002). Interestingly, these mostly differ from candidate ‘song’ genes that had been proposed by earlier work demonstrating underlying polygenic control of song.
QTL analysis is thus beginning to yield some insights into the distribution of loci influencing complex behaviour patterns, but also to throw up more questions. Depending on the complexity of the trait, however, the technique can be very demanding of time and resources. In particular, screening programmes may need to be enormous in order to achieve satisfactory statistical rigour in associating loci with traits. Furthermore, once putative QTLs have been identified, further tests are needed to pin down the genes involved.
2.4 Natural selection and ‘selfish genes’
So, the evolutionary history of behaviour can be deduced and we can demonstrate the heritable genetic basis on which such a history depends. But how has this heritable variation produced the dramatic diversity of behaviours we see today? The prevailing consensus is that most evolutionary change, certainly all adaptive evolutionary change, is driven by the process first recognised by Darwin and Wallace as natural selection. The process is easy to understand and, following Krebs & Davies (1993), can be boiled down to a handful of simple assumptions. In each case the familiar summary in terms
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