The evolutionary and developmental genetic basis of wing polyphenism in ants

Understanding the complex relationship between genotype and phenotype, and its role in generating morphological diversity, is a central issue in evolutionary biology. Studying the evolutionary and developmental genetic basis of polyphenism, which is the ability of a single genotype to develop into two or more distinct phenotypes in response to environmental contingencies, can potentially reveal important, perhaps unexpected, aspects of the genotype-phenotype relationship. Polyphenism is widespread in nature and has evolved many times independently, yet there is almost nothing known about its underlying developmental genetic architecture. In this dissertation, I examined the developmental genetic and evolutionary basis of wing polyphenism in ants. I characterized the expression of several genes within the gene network underlying the wing primordia of reproductive (winged) and sterile (wingless) ant castes. I asked three specific questions: (1) is the wing-patterning network conserved in reproductive castes; (2) where is the wing-patterning network interrupted in wingless castes; and (3) is the wing-patterning network interrupted in the same place in the wingless castes of all ant species. I found that the expression of several genes within the network is conserved in the winged castes of four ant species, whereas points of interruption within the network in the wingless castes are evolutionarily labile. The simultaneous evolutionary lability and conservation of the network underlying wing development in ants may have played an important role in the morphological diversification of this group, and may be a general feature of polyphenic development and evolution in plants and animals. To further investigate this phenomenon, I propose a conceptual and methodological framework based on the comparative method to try and distinguish the evolutionary forces responsible for driving the observed developmental and genetic changes within the wing-patterning network in wingless ant castes. The application of this methodological framework, however, requires robust phylogenetic tree of the ant species being examined. Thus, I have constructed a molecular phylogeny of 27 common North American ant species using a mitochondrial and nuclear gene. Trees based on the nuclear gene are well resolved, while trees based on the mitochondrial gene are not. This may be due to a saturation of the mitochondrial gene at this level of divergence. If rudimentary disc morphology in the wingless castes of different ant species is mapped as a trait onto these trees, then an interesting pattern emerges; rudimentary disc morphology evolves much more quickly in some subfamilies than in others. This general approach will illuminate the complex interaction between environment, genotype, and phenotype.