Landscape genomics of an obligate mutualism: discordant population structures between a leafcutter-ant and its fungal cultivars

Abstract

To explore landscape genomics at the range limit of an obligate mutualism, we used genotyping-by-sequencing (ddRADseq) to quantify population structure and the effect of hostsymbiont interactions between the northernmost fungus-farming leafcutter ant Atta texana and its two main types of cultivated fungus. At local scales, genome-wide differentiation between ants associated with either of the two fungal types is greater than the differentiation associated with the abiotic factors temperature and precipitation, suggesting that specific ant-fungus genome-genome combinations may have been favored by selection. For the ant hosts, we found a broad cline of genetic structure across the range, and a reduction of genetic diversity along the axis of range expansion towards the range margin. In contrast, genetic structure was patchy in the cultivated fungi, with no consistent reduction of fungal genetic diversity at the range margins. This discordance in population-genetic structure between ant hosts and fungal symbionts is surprising because the ant farmers co-disperse with their vertically-transmitted fungal symbionts, but apparently the fungi disperse occasionally also through between-nest horizontal transfer or other unknown dispersal mechanisms. The discordance in populationgenetic structure indicates that genetic drift and gene flow differ in magnitude between each partner in this leafcutter mutualism. Together, these findings imply that variation in the strength of drift and gene flow experienced by each mutualistic partner affects adaptation to environmental stress at the range margin, and genome-genome interactions between host and symbiont influences adaptive genetic differentiation of the host during range evolution in this obligate mutualism.