Selection against Aerial Dispersal in Ants: Two Non-Flying Queen Phenotypes in Pogonomyrmex laticeps

Christian Peeters,Robert A Johnson,Roberto A Keller

doi:10.1371/journal.pone.0047727

Abstract

The South American seed-harvester ant Pogonomyrmex laticeps has dimorphic queens: ergatoid (permanently wingless) and brachypterous (short, non-functional wings). Surveys in western Argentina indicated that colonies near Chilecito, La Rioja Province, produced only ergatoid queens, while those near Punta Balasto, Catamarca Province (263 km away), produced only brachypterous queens. Brachypterous queens were significantly larger than ergatoid queens for 10 of 11 external characters, but both phenotypes had comparable reproductive potential, i.e., a spermatheca and a similar number of ovarioles. Using normal winged queens of the closely related P. uruguayensis for comparison, we determined that both queen phenotypes in P. laticeps had a full set of dorsal thoracic sclerites, albeit each sclerite was much reduced, whereas workers had a thorax without distinct dorsal sclerites. Sclerites were fused and immobile in ergatoid queens, while they were separable and fully articulated in brachypterous queens. Both phenotypes lacked the big indirect flight muscles, but brachypterous queens retained the tiny direct flight muscles. Overall, this dimorphism across populations indicates that there are alternative solutions to selective pressures against flying queens. We lack field data about colony founding strategy (independent or dependent) for either queen phenotype, but colonies at both sites produced numerous gynes, and we infer that all foundresses initiate colonies independently and are obligate foragers.

Highlights

The sporadic but recurrent loss of flight in insects is a tantalizing evolutionary problem
Morphometric Comparison of the Female Castes Sexual castes were conspicuous during excavations at both sites: queens at Punta Balasto were callows with tiny wings (Figure 2), while ergatoid queens at Chilecito were noticeably larger than workers (Figures 3, 4)
These observations were confirmed by our morphometric analysis, which demonstrated that size of the female castes differed significantly (MANOVA: Box’s M test, F165, 10878 df = 1.19, P = 0.051; Wilks’ l = 0.017, F30, 241 = 24.4, P, 0.0001); all 10 continuous characters varied among castes

Summary

Introduction

The sporadic but recurrent loss of flight in insects is a tantalizing evolutionary problem. Ability to fly is a tremendous adaptation that enhances dispersal, location of scattered resources (food and mates), and avoidance of predators In species such as bees and dragonflies, flight is an integral part of daily life, while in other insects it only serves as a mechanism for dispersal. Unlike other eusocial Hymenoptera, ants have a permanently wingless worker caste, such that both winged and wingless females are produced in the same colony Even this highly reduced function of flight has been lost numerous times and ergatoid (permanently wingless) queens occur in species belonging to most subfamilies of ants [5]. It is generally thought that flightcapable queens are selected against when the energetic or mortality costs of long-distance dispersal outweigh the benefits of colonizing disjunct habitats

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Conclusion