Dynamics of an ant-ant Obligate Mutualism: Colony Growth, Density Dependence and Frequency Dependence

Authors: Anderson, Kirk; WHEELER, DIANA - University Of Arizona; YANG, KIMBERLY - University Of Arizona; LINKSVAYER, TIMOTHY - University Of Copenhagen

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/20/2011
Publication Date: 6/20/2011
Citation: Anderson, K.E., Wheeler, D., Yang, K., Linksvayer, T. 2011. Dynamics of an ant-ant obligate mutualism: Colony growth, density dependence and frequency dependence. Molecular Ecology. 20:1781-1793.

Interpretive Summary: Typically, the fertilized eggs of ants and honey bees develop into a queen or a worker according to the type of nutrition. In some harvester ants however, this process occurs according to the genetic predisposition of the egg, and involves two separate species that must hybridize with one another to produce workers. This breeding system imposes subsequent costs and benefits for each species that depend on the ratios of each species in the system. We surveyed the lineage ratios of 49 systems across the range of the occurrence and found that the global lineage frequency differed significantly from equal. The species respond differently to environmental conditions; one species increases in frequency with colony density. While the queens early colony founding success depends on the amount of worker-destined sperm she acquires during mating, subsequent colony growth is independent of this factor and differs between the species. Collectively, these findings suggest that a combination of lineage ratios, environmental variables and species-specific traits govern the dynamics of the system.

Technical Abstract: In insect societies, worker versus queen development (reproductive caste) is typically governed by environmental factors, but many Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Same-lineage matings produce fertile queens while alternate-lineage matings produce sterile workers. Because new virgin queens mate randomly with multiple males of each lineage type, and both worker and queen phenotypes are required for colony growth and future reproduction, fitness is influenced by the relative frequency of each lineage involved in the mutualistic breeding system. While models based solely on frequency dependent selection predict the convergence of lineage frequencies toward equal (0.5/0.5), we surveyed the lineage ratios of 49 systems across the range of the mutualism and found that the global lineage frequency differed significantly from equal. Multiple regression analysis of our sustem survbey data revealed that the frequency of one lineage increases at higher altitudes, while the frequency of the alternate lineage increases with colony density. While the queens colony founding sucdess is largely frequency dependent, relying on the random acquisition of worker-biased sperm stores, subsequent colony growth is independent of lineage frequency. We provide a simulation model showing that a net ecological advantage held by one lineage can lead to the maintenance of stable but asymmetric lineage frequencies. Collectively, these findings suggest that a combination of frequency-dependent and frequency-independent mechanisms can generate many different localized and independently evolving system equilibria.