The maintenance of polymorphism by behavioral and genomic plasticity in mate preference

The maintenance of genetic variation in traits that are closely tied to fitness, despite evolutionary forces expected to reduce variation, is a long-standing paradox in evolutionary biology. Under simple population genetic models, genetic variation will be determined by a balance between the input of new variation through mutation and the elimination of variation by selection and genetic drift; however, the ability of these forces to generate and maintain the high variation found in natural populations is a continuing debate. Frequency-dependent selection can maintain extensive variation in natural populations well above the levels predicted by simple population genetic models. In the Trinidad guppy, Poecilia reticulata, negative frequency-dependent selection through a female preference for rare or novel mates is one proposed mechanism maintaining the extreme color polymorphism seen in wild populations. Despite the apparent generality of a female mating preference for novel color patterns in this species, the evolutionary origin of the novel mate preference remains unknown. One hypothesis for the origin of the novel mate preference is that guppies have been selected for increased responsiveness to novel stimuli for reasons unrelated to mating. If response to novel stimuli leads to a selective advantage, such as a competitive foraging advantage, then the novel mate preference could be a pleiotropic side-effect of selection for increased efficiency in foraging.;To determine whether the novel mate preference is due to a generalized preference for novel stimuli, I conducted two experiments. In the first experiment, I examined the molecular changes occurring in female brains when exposed to a male with a novel versus a familiar color pattern. If mate preference for novel coloration is a byproduct of a general preference for novelty, I predicted that genes previously implicated in novelty-seeking would be differentially expressed in females exposed to males with novel compared to familiar color patterns. While I did find genes specifically related to novelty-seeking, I found over 150 other genes that were differentially expressed between the novel and familiar behavior treatments, suggesting that female perception of novel mates is physiologically complex and is correlated with a series of transcriptional changes. In the second experiment, I examined the preference for novel environmental stimuli. I compared the behavioral responses of guppies exposed to novel versus familiar objects and novel versus familiar food sources. Overall, neither male nor female guppies demonstrated a strong preference for environmental novelty.;In a third experiment, I examined the mating patterns in a species closely-related to the guppy, Poecilia picta. I conducted a series of experiments to determine whether P. picta show a preference for rare males or males with novel color patterns. While I did not find a female preference for males that exhibited the locally rare color pattern found in natural populations, I did determine that female P. picta show a preference for males with novel color patterns. Results of this study suggest that negative frequency-dependent selection is operating in P. picta, and potentially plays a role in the maintenance of color polymorphism in this species.;In conclusion, my results do not provide consistent, strong support that the female guppy novel mate preference originated from a bias for generalized novelty. I do, however, identify neurogenomic changes associated with novel mate preference and provide the first demonstration of the mating patterns in a polymorphic P. picta population. Overall, the work outlined in this dissertation provides unique insight into the behavioral and genomic mechanisms driving genetic variation across Poeciliid species.