The Genetics of Behavior

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To say that behavior is inherited does not mean that specific genes code for specific behaviors. Genes code for proteins, and there are many complex steps between the expression of a gene as a protein product and the expression of a behavior. In no case are all the steps between a gene and its influence on a behavior known. Nevertheless, it is clear that behavior has genetic determinants. In this section we will look at three approaches to investigating how genes affect behavior: hybridization, artificial selection and crossing of the selected strains, and molecular analysis of genes and gene products.

Hybridization experiments show whether a behavior is genetically determined

The effects of hybridization on the courtship displays of dabbling duck species were the subject of a classic ethological experiment, as we saw above. A more recent set of hybridization experiments was performed on crickets. The songs of crickets, like bird songs, are species-specific, and as in birds, only male crickets "sing." They do so by rubbing one wing against another wing that has a serrated edge. The sounds they produce can be recorded and analyzed quantitatively.

When two species of crickets were crossed, their offspring (the Fj generation) expressed songs that had features of the songs of both parental species. Backcrosses of Fj in

Male canary

Testosterone induces growth in the regions responsible for song.

dividuals with the parental species produced individuals that had songs closer to that of the parental species used in the backcross. Clearly the genetic background determined the song pattern. What was amazing, however, was the demonstration that female preferences for male songs were under similar genetic control. Given a choice, females from each parental species preferred the calls of males from their own species, but hybrid females preferred the calls of hybrid males.

These genetic differences between the two parental cricket species and the hybrids were reflected in the properties of their nervous systems. When specific neurons in the crickets' brains were stimulated, songs that reflected the genotypes of the crickets were expressed.

Artificial selection and crossbreeding experiments reveal the genetic complexity of behavior

Domesticated animals provide abundant evidence that artificial selection of mating pairs on the basis of their behavior can result in strains with distinct behavioral as well as anatomical characteristics. Among dogs, consider retrievers, pointers, and shepherds. Each has a particular behavioral tendency that can be honed to a fine degree by training. However, dogs and other large animals are not the best subjects for genetic studies. Most artificial selection experiments in behavioral genetics have been done on more convenient laboratory animals with short life cycles and large numbers of offspring, such as the fruit fly (Drosophila).

Artificial selection has been successful in shaping a variety of behavior patterns in fruit flies, especially aspects of their courtship and mating behavior. Crossing of these artificially selected strains reveals that most of these behavioral differences are due to multiple genes that probably influence the behavior indirectly by altering general properties of the nervous system.

Few behavioral genetic studies reveal simple Mendelian segregation of behavioral traits. An exception is nest-cleaning behavior in honeybees. One genetic strain of honeybees practices nest-cleaning, or hygienic, behavior, which makes them resistant to a bacterium that infects and kills the larvae of honeybees. When a larva dies, workers of this strain uncap its brood cell and remove the carcass from the hive. Another strain of honeybees does not show this hygienic behavior and therefore is more susceptible to the spread of the disease (Figure 52.9).

When these two strains of honeybees were crossed, all members of the F1 generation were nonhygienic, indicating that the behavior is controlled by recessive alleles. Back-crossing the F1 with the hygienic parental strain produced the typical 3:1 ratio expected for a two-gene trait in the F2 generation (see Chapter 10). The behavior of the nonhygienic F2 individuals was also interesting. One-third of them showed no hygienic behavior at all; one-third uncapped the cells of dead larvae, but did not remove them; and one-third did not uncap cells, but did remove carcasses if the cells were open.

Even though these results suggest a gene for uncapping and a gene for removal, these behavior patterns are complex. They involve sensory mechanisms, orientation movements, and motor patterns, each of which depends on multiple properties of many cells. The genetic deficits of nonhygienic bees could influence very small, specific, yet critical properties of some cells. If even a single critical prop-

52.9 Genes and Hygienic Behavior in Honeybees Some honeybee strains remove the carcasses of dead larvae from their nests.This behavior seems to have two components: uncapping the larval cell (u) and removing the carcass (r),each of which is under the control of a recessive gene.

Nonhygienic bees

Hygienic bees -

Parental generation

Genotype of females Genotype of males Gametes (male or female)

Fj (all nonhygienic)

Genotype of females Gametes produced by females

Backcross to males of hygienic strain

F2 generation females

Genotypes Behaviors

Nonhygienic bees

Hygienic bees -

Genotype of females Genotype of males Gametes (male or female)

uu is the "uncap" gene. rr is the "remove" gene.

UuRr

Hygienic bees uncap cells and remove the dead larvae.

uu is the "uncap" gene. rr is the "remove" gene.

UuRr

F2 generation females

UuRr Nonhygienic

Uurr uuRr uurr Hygienic

These bees are nonhygienic, but will remove dead larvae if cells are uncapped.

These bees are nonhygienic. They will uncap cells of dead larvae, but won't remove them.

erty, such as a crucial synapse or a particular sensory receptor, were lacking, the whole behavior pattern would fail to be expressed. Thus there is no specific gene that codes for the entire behavior.

Molecular genetic techniques reveal specific genes that influence behavior

Molecular geneticists are investigating specific genes that influence behavior. Male courtship behavior in fruit flies is a subject of many such studies. This behavior is stereotypic, species-specific, and requires no learning. A male recognizes a potential mate, follows her, taps her body with his forelegs, extends and vibrates one wing, and licks the female's genitals. If the female is receptive, the male copulates with her (Figure 52.10a). Research in molecular genetics has now shown that most of this male courtship behavior is controlled by a single gene.

In fruit flies with two X chromosomes (females), a gene called sex-lethal (sxl) is expressed. This gene is at the top of a genetic hierarchy that determines all aspects of sexual dif-

ferentiation and behavior in fruit flies (Figure 52.10b). The Sxl protein causes another gene, called transformer (tra), to produce the female-specific Tra protein. Fruit flies without the tra gene develop into males anatomically and behaviorally, regardless of how many X chromosomes they have. But it is still another gene in the sex determination hierarchy that is responsible for male behavior.

In the absence of the Tra protein, two additional genes, called doublesex (dsx) and fruitless (fru), are expressed. The dsx gene controls the anatomical differentiation of males, and fru causes the formation of a nervous system that expresses male courtship behavior. Mutations of the fru gene do not affect male body form, but they disrupt male courtship behavior. We don't know all of the actions that the male-specific Fru protein has in the development of the fruit fly nervous system, but this is about as close as we can get at present to identifying a gene that controls a complex behavior.

52.10 The fruitless Gene Controls Male Courtship Behavior in Fruit Flies (a) Male fruit flies display stereotypic, species-specific courtship behavior. (b) Sexual differentiation in Drosophila is controlled by a hierarchy of genes; in that hierarchy, fru controls the branch that leads to male courtship behavior.

52.10 The fruitless Gene Controls Male Courtship Behavior in Fruit Flies (a) Male fruit flies display stereotypic, species-specific courtship behavior. (b) Sexual differentiation in Drosophila is controlled by a hierarchy of genes; in that hierarchy, fru controls the branch that leads to male courtship behavior.

Hierarchy Control Maritime

Orienting

Tapping

Wing vibration

Licking

Attempted

Copulation

Sex-determining pre-mRNAs are spliced in one specific way in female flies.

Orienting

Tapping

Wing vibration

Licking

Attempted

Copulation

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