ANT MUTUALISM AND THE EVOLUTION OF PARENTAL CARE IN TREEHOPPERS: INTEGRATING BEHAVIORAL ECOLOGY, COMPARATIVE GENOMICS, AND PHYLOGENETIC HISTORY

Abstract

Parental care is central to the biology of many animals and has evolved many times independently, but the ecological factors and the evolutionary processes driving the origin and loss of parental care remain poorly understood. Treehoppers – phloem-feeding insects comprising the three hemipteran families Aetalionidae, Melizoderidae, and Membracidae – are an excellent system for addressing the causes and consequences of the origin of parental care because female egg guarding has been gained and lost many times in different lineages. A fulcrum of treehopper ecology is ant attendance, where ants protect treehopper adults and nymphs in exchange for honeydew, a byproduct of phloem-feeding. Ant attendance has likewise been gained and lost many times, providing a window into how the phylogenetic history of ecology has influenced the evolution of parental care. This cross-species diversity in ecology and life history is highly amenable to comparative analysis, and it is also recapitulated by within- population plasticity amenable to field experiments and quantification of the adaptive value of different care tactics. Here, I leverage this phylogenetic history and plasticity to test hypotheses about the ecological and molecular causes and consequences of parental care evolution. In Chapter 1, I use an ant-exclusion field experiment to investigate the factors shaping parental care decisions in Publilia reticulata and measure the consequences on lifetime fitness. I show that mothers offload egg guarding onto conspecific females and nymph guarding onto “ant nannies” when available, but the fitness payoffs of each strategy depend on fecundity. In Chapter 2, I use comparative genomics to identify the genes and pathways under selection during the evolution of egg guarding and ant attendance. I find that maternal care evolution, but not ant attendance evolution, has coincided with genome-wide pervasive relaxation of selection, likely due to shifts in selective regimes rather than changes in demography associated with the evolution of social behavior in other taxa. In Chapter 3, I generate and leverage the most taxonomically comprehensive phylogeny and behavior database to reconstruct the gains of maternal care and losses of ant attendance, confirming the hypothesis that ant attendance has repeatedly promoted the origin of maternal care in treehoppers.