Interspecific Hybridization in the Seed-Harvester Ant <em>Pogonomyrmex</em> (Hymenoptera: Formicidae): Evidence for a Mosaic Hybrid Zone

Seed-harvester ants are best known for building large gravel mounds, "harvesting" the seeds of favorite grasses, and delivering a most painful sting. Early naturalists observed favored grasses and other annual plants surrounding the gravel mounds, and concluded that the ants had planted seeds close to home to expedite the summer harvest. These rusty-red and highly organized colonial insects guard their mounds with an altruistic ferocity rarely seen in the natural world. North American seed-harvester ants include the genus Pogonomyrmex, (bearded-ant) which is a moderate sized New World genus consisting of about 48 species, 25 of these occurring in North America. The more primitive South American species suggest that the genus evolved in South America and later migrated to, and radiated in North America. Typical life history of Pogonomyrmex begins with the mating flight and extremely high levels of mortality for newly-mated queens (» 99%). Once colonies become established (1-2 years), mortality decreases dramatically and colonies can survive for 15-30 years. Large and mature colonies (3-5 years) produce hundreds of sexuals each year, and the mating flights of most species are triggered by summer rains. Generally, Pogonomyrmex are highly specialized strict granivores, though insects are readily taken when available. Seeds are stored in chambers below the surface and foraging is limited to daily periods of relatively moist and cool conditions. Pogonomyrmex occidentalis and P. maricopa belong to very different and monophyletic species complexes, with species from each complex generally affiliated with particular geographic regions. The P. occidentalis complex consists of six species all of which are primarily restricted to higher latitudes in the United States and southern Canada, typically at mid to high elevations. The P. maricopa complex contains eight species that occur at low latitudes of the United States and Mexico from low to mid elevations. Pogonomyrmex occidentalis inhabits cool deserts and grasslands, is abundant between 4000-8700 ft. in sagebrush steepe of the Great Basin Desert, and sporadically distributed above 5500 ft. in the hot deserts on "sky islands". Pogonomyrmex maricopa inhabits arid-regions, is common at low elevations in the Mojave, Sonoran, and Chihuahuan Deserts, and is generally found between 500-4500 ft. elevation. In the Virgin River basin and Zion National Park, the ranges of these two highly distinct species overlap in an ecological transition zone. In this "hybrid zone" the hybrid colonies show a broad range of morphological intermediacy, possess additive parental RAPD markers, occupy intermediate soils and climates, and construct nests with structures intermediate between parental P. occidentalis and P. maricopa nests. I examined the morphology of colonies and populations across and within the hybrid zone to establish a geographical pattern of hybridization. I used neutral genetic markers (RAPDs) to provide decisive evidence of hybridization, and reveal patterns of introgression not indicated by the morphological hybrid index. Ecological data were compared with morphological principle component scores as a means of correlating ecological parameters with the pattern of hybridization. Mound shape was examined relative to colony soil texture and parental morphology. Emerging patterns were compared to three accepted hybrid zone models. Eight morphological characters were fixed or nearly invariable in each of the putative parental species, and were highly variable in the putative hybrid, showing a broad spectrum of intermediacy. A hybrid index and principal components analysis both suggest the intermediate placement of the putative hybrid. Individual character frequencies plotted against distance from the center of the hybrid zone show steep and coincident clines, indicating a secondary contact zone. A Tukey's multiple comparison test on principle component scores revealed significant differences between populations within the hybrid zone indicating the structure of a mosaic hybrid zone and suggesting different selection regimes. Slight clinal asymmetry across the hybrid zone, and significant differences between hybrid zone P. maricopa and allopatric P. maricopa suggest extensive backcrossing or highly localized introgression of P. occidentalis genes into P. maricopa. An initial survey of 120 RAPD primers revealed 14 diagnostic parental species markers, which were used to describe the structure of the hybrid zone. RAPD analyses produced strong evidence for the interspecific hybrid origin of all morphologically putative hybrids. Morphological P. maricopa in the western half of the hybrid zone shared more RAPD markers with P. occidentalis than did allopatric P. maricopa indicating highly localized introgression of genes from P. occidentalis into P. maricopa. Clines from RAPD markers were coincident and concordant, showing the same general shape and placement as morphological clines, suggesting an environment by genotype association. The soil textures from colonies in the Great Basin, Virgin River Basin, and the Mojave Desert were significantly different among all three areas. Morphological principle component scores from hybrid colonies were correlated with clay and precipitation within the hybrid zone suggesting selection for desiccation tolerance among hybrid phenotypes. Percent clay was the soil texture class showing the strongest positive correlation with morphology between ecosystems and within the hybrid zone. Temperature was significant between ecosystems, but not between populations within the hybrid zone, suggesting that this variable serves to limit the distribution of the parental species over broad geographical regions. Hybridization patterns are characteristic of secondary contact between previously allopatric forms, and correspond to the mosaic model of a hybrid zone, where parent species and hybrids are adapted to different patchily distributed environments. Based on distribution patterns, hybrid colonies seem better adapted than either parent to the intermediate environment of the hybrid zone, and apparently retain the potential to produce novel and adaptive genotypes, adding to the skepticism that speciation occurs through reinforcement, and challenging the idea that animal hybridization in is an evolutionary dead-end.

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