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Part III

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FROM NEURAL CIRCUIT EVOLUTION TO ADAPTIVE BEHAVIOR

The five chapters of Part III aim to link evolutionary changes in neural circuits to the evolution of behavior. In Chapter 9, James Newcomb and colleagues describe the neural circuits underlying swimming behavior in various Nudipleura (sea slugs). As it turns out, some nudipleuran species have evolved the ability to swim by undulating their bodies either from side to side or dorsoventrally. Importantly, these different types of swimming evolved independently in several different lineages, allowing for interesting comparisons of their underlying circuitry. Specifically, Newcomb et al. report that nonhomologous swimming behaviors can be mediated by neural circuits that include homologous (as well as nonhomologous) neurons and that clearly homologous swimming in closely related species may involve nonhomologous neurons. These findings show that, even for homologous behaviors, it is difficult to predict how conserved the underlying circuits are. An important implication of this finding is that one cannot homologize behaviors merely on the basis of how similar their underlying circuits are. This conclusion extends a theme first mentioned by Northcutt (Chapter 3): homology at one level of biological organization need not imply homology at other hierarchical levels.

In Chapter 10, Andrew Bass and Boris Chagnaud review the literature showing that the premotor neurons controlling sound production tend to be derived from caudal rhombomere 8 in the hindbrain of many different vertebrates, including fishes and amphibians. Something about these neurons makes them especially well suited for complex, often rhythmic, pattern generation and for the coordination of diverse muscles, including



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Part III FROM NEURAL CIRCUIT EVOLUTION TO ADAPTIVE BEHAVIOR T he five chapters of Part III aim to link evolutionary changes in neural circuits to the evolution of behavior. In Chapter 9, James Newcomb and colleagues describe the neural circuits underlying swimming behavior in various Nudipleura (sea slugs). As it turns out, some nudipleuran species have evolved the ability to swim by undulating their bodies either from side to side or dorsoventrally. Importantly, these different types of swimming evolved independently in several different lineages, allowing for interesting comparisons of their underlying cir- cuitry. Specifically, Newcomb et al. report that nonhomologous swimming behaviors can be mediated by neural circuits that include homologous (as well as nonhomologous) neurons and that clearly homologous swimming in closely related species may involve nonhomologous neurons. These findings show that, even for homologous behaviors, it is difficult to predict how conserved the underlying circuits are. An important implication of this finding is that one cannot homologize behaviors merely on the basis of how similar their underlying circuits are. This conclusion extends a theme first mentioned by Northcutt (Chapter 3): homology at one level of bio- logical organization need not imply homology at other hierarchical levels. In Chapter 10, Andrew Bass and Boris Chagnaud review the literature showing that the premotor neurons controlling sound production tend to be derived from caudal rhombomere 8 in the hindbrain of many differ- ent vertebrates, including fishes and amphibians. Something about these neurons makes them especially well suited for complex, often rhythmic, pattern generation and for the coordination of diverse muscles, includ- 149

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150 / Part III ing the muscles related to breathing. Bass and Chagnaud further point out that in toadfishes the hindbrain vocal motor neurons lie adjacent to motor neurons innervating the pectoral fins. This finding suggests that the neural circuitry for sound production shares a long evolutionary (and developmental) history with the circuits controlling the pectoral fins and, in tetrapods, the forelimbs. This hypothesis may seem far-fetched at first; however, pectoral fins are used for sound production in a number of fishes, and forelimbs are clearly used for gestural communication in humans. If correct, the hypothesis implies a deep homology between behaviors that seem quite disparate but involve homologous neural circuits and, presum- ably, homologous developmental genes. James Goodson and colleagues in Chapter 11 examine variation in neuropeptide expression across multiple brain regions involved in avian social behavior. More specifically, the paper focuses on differences in peptide expression among four emberizid songbird species, examining their correlation with seasonal changes in territoriality and/or flocking behavior. The analysis gets complicated, because variation in the degree of territoriality may be caused by reduced aggression or increased gregari- ousness (i.e., flocking), which likely involve different neural mechanisms. However, clever species selection allows the authors to identify one set of differences in neuropeptide expression that is most likely linked to dif- ferences in aggression and another set that correlates with differences in flocking behavior. As the authors admit, the conclusions are based on just a few species and, therefore, tentative. However, the study undeniably reveals an unexpectedly large degree of variation in peptide levels both across species and within species (i.e., seasonal variation). This variation is probably a driving force behind the variation in behavior, although it may also be a consequence. Experimental manipulations are needed to discriminate between these two hypotheses. In Chapter 12, Lucia Jacobs develops ideas about the role of the hip- pocampus in navigation. She suggests that olfaction played a crucial early role in the evolution of spatial orientation, providing information about spatial gradients (in odor plumes) as well as local cue constellations (locale-specific odorant mixtures). The hippocampus became specialized to process and integrate these two kinds of information. Subsequently, these functions were extended to other sensory modalities. An interesting corollary of this hypothesis is that the size of the olfactory system should correlate more tightly with an organism’s ability to navigate by olfac- tory cues than with its capacity for odor discrimination. The hypothesis might also explain why olfactory brain regions scale less tightly than other regions with overall brain size. Perhaps the evolutionary shift to multimodal navigation allowed the olfactory system to be reduced. Jacobs predicts that the olfactory system should be larger in species that must

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From Neural Circuit Evolution to Adaptive Behavior  /  151 predict when and where their food will be available than in species that feed opportunistically. In Chapter 13, Kenneth Catania reports on two natural but highly unusual feeding behaviors. First, Catania reviews the incredibly rapid and efficient hunting behavior of star-nosed moles. Using optimal forag- ing theory, he shows that these small predators are specialized for rapidly finding and eating small aquatic invertebrates. Their star-shaped “nose” evolved to help them in this task, as did a series of related specializations in the brain, including an expanded somatosensory cortex. Catania then turns to an aquatic snake that has evolved a fascinating trick for catching fish. It uses a tiny muscular contraction of its body to trigger a nearby fish’s escape response in such a way that the hapless fish tends to swim directly into the snake’s wide-open fangs. Even more remarkable, the snakes can anticipate the trajectory of the escape response, intercepting a fish before it gets away. Because this predictive ability is found even in naive snakes that have never caught (or missed catching) a fish, it seems to be innate (i.e., unlearned). Why did the fish retain their stereotyped escape response, given that the snakes can exploit it? The answer may be that snakes are relatively rare, and the escape response serves the fish well when dealing with most other threats.

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