Phylogeography of Pogonomyrmex barbatus and P. rugosus harvester ants with genetic and environmental caste determination

Authors: Mott, Brendon; GADAU, JURGEN - Arizona State University; Anderson, Kirk

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/5/2015
Publication Date: 7/1/2015
Citation: Mott, B.M., Gadau, J., Anderson, K.E. 2015. Phylogeography of Pogonomyrmex barbatus and P. rugosus harvester ants with genetic and environmental caste determination. Ecology and Evolution. 5(14):2798-2826. DOI: 10.1002/ece3.1507

Interpretive Summary: Modern DNA analysis methods have repeatedly challenged biologists to rethink the evolutionary relationships among and within species. Studies with phylogenetic and population genetics methods have shown that some nominal species, which were historically grouped together because of common physical or behavioral characteristics, are actually composed of many distinct subgroups. In other cases, such studies have found that two closely related species are actually capable of hybridizing where their distributions meet. Thus, studying the phylogenetic and geographic patterns within and among closely related species provides both a snapshot of their current diversity and a window into their historical demographics and distributions. This information on the historical changes in a species can be paired with paleoclimatology and historical geology to infer relationships between changes in physical geography, climate, and biological communities. This study focuses on two nominal species of North American seed-harvester ants. These ants are known to have a complex history of hybridization and some unique genetic incompatibilities that make them an interesting model for a variety of questions on speciation and developmental genetics, but some of these questions cannot be answered until we understand their phylogenetic history. In addition, there are very few phylogeograpy studies on invertebrates in the North American deserts, and no such studies on ants, so there are many questions remaining on the degree to which different insect groups may have been influenced by geographic and climatological changes in the Pliocene, Pleistocene, and Holocene epochs. This study identifies the hybrid parents of several key groups, indicating that ant populations in Mexico, not the U.S., are probably the most closely related ancestors to the lineages with unique genetic incompatibilities. This information helps us interpret previous studies on this system, and it should assist future researchers that wish to investigate the hybrid origins of these groups. Moreover, this is the first study to describe genetic diversity across the complete range of these two species and their various subgroups. Combined with estimates of their evolutionary age and various sources of paleoclimatological and geological data, this study confirms that many, but not all, of the patterns found in vertebrates are also found in these arid-adapted harvester ants. These results provide additional data on the evolution of the ancient deserts, and they should provide a model for future studies on arid-adapted insects in these regions.

Technical Abstract: Here we present a phylogeographic study of at least six reproductively isolated lineages of new world harvester ants within the Pogonomyrmex barbatus and P. rugosus species group. The genetic and geographic relationships within this clade are complex: four of the identified lineages are divided into two pairs, and each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because interlineage matings within each pair are the sole source of hybrid F1 workers; these workers build and sustain the colonies, facilitating the production of the reproductive caste, which results solely from intralineage fertilizations. This system of genetic caste determination (GCD) maintains genetic isolation among these closely related lineages, while simultaneously requiring co-expansion and emigration as their distributions have changed over time. It has also been demonstrated that three of these four GCD lineages have undergone historical hybridization, but the narrower sampling range of previous studies has left questions on the hybrid parentage, breadth, and age of these groups. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and hypotheses, and to plan future inquiries in a more complete historical biogeographic context. Using mitochondrial DNA sequences sampled across most of the morphospecies' ranges in the U.S. and Mexico, we employed several methods of phylogenetic and DNA sequence analysis, along with comparisons to geological, biogeographic, and phylogeographic studies throughout the sampled regions. Interestingly, our results indicate that one of the GCD lineage pairs have experienced a dramatic range expansion, despite the predicted fitness costs of the GCD system. However, the broader analyses reveal a complex pattern of vicariance and dispersal in Pogonomyrmex harvester ants that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid-adapted taxa in North America.