Lateralized Feeding Behavior is Associated with Asymmetrical Neuroanatomy and Lateralized Gene Expressions in the Brain in Scale-Eating Cichlid Fish

Recent evidence in natural and semi-natural settings has revealed a variety of left-right perceptual asymmetries among vertebrates. These include preferential use of the left or right visual hemifield during activities such as searching for food, agonistic responses, or escape from predators in animals as different as fish, amphibians, reptiles, birds, and mammals. There are obvious disadvantages in showing such directional asymmetries because relevant stimuli may be located to the animal's left or right at random; there is no a priori association between the meaning of a stimulus (e.g., its being a predator or a food item) and its being located to the animal's left or right. Moreover, other organisms (e.g., predators) could exploit the predictability of behavior that arises from population-level lateral biases. It might be argued that lateralization of function enhances cognitive capacity and efficiency of the brain, thus counteracting the ecological disadvantages of lateral biases in behavior. However, such an increase in brain efficiency could be obtained by each individual being lateralized without any need to align the direction of the asymmetry in the majority of the individuals of the population. Here we argue that the alignment of the direction of behavioral asymmetries at the population level arises as an "evolutionarily stable strategy" under "social" pressures occurring when individually asymmetrical organisms must coordinate their behavior with the behavior of other asymmetrical organisms of the same or different species.

We show that the age-related transition by adult honey bees from hive work to foraging is associated with changes in messenger RNA abundance in the brain for 39% of approximately 5500 genes tested. This result, discovered using a highly replicated experimental design involving 72 microarrays, demonstrates more extensive genomic plasticity in the adult brain than has yet been shown. Experimental manipulations that uncouple behavior and age revealed that messenger RNA changes were primarily associated with behavior. Individual brain messenger RNA profiles correctly predicted the behavior of 57 out of 60 bees, indicating a robust association between brain gene expression in the individual and naturally occurring behavioral plasticity.

Frequency-dependent natural selection has been cited as a mechanism for maintaining polymorphisms in biological populations, although the process has not been documented conclusively in field study. Here, it is demonstrated that the direction of mouth-opening (either left-handed or right-handed) in scale-eating cichlid fish of Lake Tanganyika is determined on the basis of simple genetics and that the abundance of individuals with left- or right-handedness depends on frequency-dependent natural selection. Attacking from behind, right-handed individuals snatched scales from the prey's left flank and left-handed ones from the right flank. Within a given population, the frequency of the two phenotypes oscillated around unity. This phenomenon was effected through frequency-dependent selection exerted by the prey's alertness. Thus, individuals of the rare phenotype had more success as predators than those of the more common phenotype.