Corresponding author: Jackson A. Helms IV ( firstname.lastname@example.org )
Academic editor: Robert Colautti
© 2017 Jackson A. Helms IV, Eli S. Bridge.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Helms IV JA, Bridge ES (2017) Range expansion drives the evolution of alternate reproductive strategies in invasive fire ants. NeoBiota 33: 67-82. https://doi.org/10.3897/neobiota.33.10300
Many species are expanding their ranges in response to climate changes or species introductions. Expansion-related selection likely drives the evolution of dispersal and reproductive traits, especially in invasive species introduced into novel habitats. We used an agent-based model to investigate these relationships in the red imported fire ant, Solenopsis invicta, by tracking simulated populations over 25 years. Most colonies of this invasive species produce two types of queens practicing alternate reproductive strategies. Claustral queens found new colonies in vacant habitats, while parasitic queens take over existing colonies whose queens have died. We investigated how relative investment in the two queen types affects population demography, habitat occupancy, and range expansion. We found that parasitic queens extend the ecological lifespan of colonies, thereby increasing a population’s overall habitat occupancy as well as average colony size (number of workers) and territory size. At the same time, investment in parasitic queens slowed the rate of range expansion by diverting investment from claustral queens. Divergent selection regimes caused edge and interior populations to evolve different levels of reproductive investment, such that interior populations invested heavily in parasitic queens whereas those at the edge invested almost entirely in claustral queens. Our results highlight factors shaping ant life histories, including the evolution of social parasitism, and have implications for the response of species to range shifts.
Agent-based Model, Dispersal Evolution, Dispersal Polymorphisms, Invasions, Reproductive Polymorphisms, Range Expansion, Social Parasitism, Solenopsis invicta
Many species throughout the world are shifting or expanding their ranges in response to climate changes or species introductions (Parmesan et al. 1999,
Ants present some of the world’s most conspicuous recent range expansions. Many species are global invasives whose non-native ranges are expanding through natural and human-assisted dispersal (
The red imported fire ant (Solenopsis invicta), perhaps the best-known invasive ant, is an ideal organism for examining these relationships. It is native to South America but was accidentally introduced to the southeastern USA in the 1930s and to several other countries afterward (
Using S. invicta as a model, this study addresses two questions related to range expansion and alternative reproductive strategies. The first question, posed from the perspective of a population ecologist, asks how investment in parasitic queens affects the spatial distributions of fire ant populations with regard to colony size (number of workers in a colony), territory size (area controlled by a colony), and the propensity to expand into suitable habitats. The second question takes an evolutionary perspective and asks what the optimal relative investment in the two strategies is for colonies seeking to maximize their contribution to future generations.
The presence of parasitic queens in a population makes colonies potentially immortal. Genetic lineages within a colony are replaced over time as queens die and new ones take over. But the colony itself may remain on the landscape for generations, as long as it is successfully parasitized every time it is orphaned. This scenario prompted us to conceive the Immortality Hypothesis, which entails three predictions associated with extending the ecological lifespan of colonies. First, parasitic queens should increase the average colony size in a landscape. Second, parasitic queens should increase occupancy of the habitat by fire ant colonies (
From the perspective of a reproductive queen, the optimal investment in daughters practicing the two strategies probably varies with location. Colonies at an expanding edge should experience more reproductive success by investing heavily in claustral daughters that can colonize empty habitat. On the other hand, colonies in the saturated range interior should benefit more from investment in parasitic daughters, as empty habitat is scarce and there are plenty of established colonies with recently deceased queens. Under what we call the Optimal Investment Hypothesis, relative investment in claustral versus parasitic queens should evolve as populations expand. In particular, the average investment in claustral queens should increase from the core to the range edge.
We evaluate these hypotheses using an agent-based computer model to track dispersal and colony founding in expanding fire ant populations over 25 years. To examine the ecological effects of reproduction-dispersal polymorphisms, we compare demography, habitat occupancy, and range expansion among populations differing in relative investment in claustral versus parasitic queens. To examine fitness implications of the two strategies, we monitor changes in relative investment within a single variable population as it expands. While we focus on the dynamics of range shifts, our results also provide insight into factors shaping the evolution of reproductive strategies in ants.
We constructed an agent-based model in the program R (
Example simulation of a mixed population consisting of several lineages. a Simulation after 0 months, showing starting conditions b after 22 months, after the first season of dispersal c after 34 months, showing orphaned colonies (gray); and d 300 months, at the end of the simulation. Simulation arenas are 50 meters wide. Colors represent lineages that invest different amounts of effort in claustral versus parasitic queens.
We ran two sets of simulations, the first to examine the effects of reproductive polymorphisms on populations, and the second to examine the fitness implications for colonies investing in the two reproductive strategies. For the first set of simulations, we seeded arenas with 50 colonies that all invested the same amount of effort in claustral versus parasitic queens. We then ran each simulation for 300 months (25 years). Each simulation represented one of six treatments, wherein the proportion of effort that colonies invested in claustral queens was set to 1, 0.98, 0.95, 0.90, 0.75, or 0.50. We ran 72 simulations for each treatment using a C4.8xlarge virtual computer available through Amazon Web Services, which allowed us to run 36 simulations at a time. After accounting for failed simulations (see Appendix
For each simulation in this first set, we measured the average colony size, average territory size, percentage of available area occupied by all colonies, percentage of colonies headed by parasitic queens, and the maximum upward extent of the range. The upward extent was defined by the maximum y-coordinate among all the territory outlines. To examine spatial patterns we divided the occupied area into sampling windows that were 5 meters high in the up-down axis and extended across the 50-meter width of the arena. We focused on colony size rather than age, because in fire ants (and other social insects) a colony’s size is a better indicator of its ecological impact and reproductive potential. Moreover, a colony’s size at any age can vary over orders of magnitude due to environmental factors and competitive interactions (
The second set of simulations investigated fitness and optimal investment of colonies producing the two queen types. For these simulations, we seeded each arena with 50 colonies varying in relative claustral investment. Each of five levels of investment—0.98, 0.95, 0.90, 0.75, and 0.5—was represented by 10 starting colonies, yielding an initial average claustral investment of 0.847. We then ran the simulation for 300 months (25 years), allowing average claustral investment to evolve through the differential survival and reproduction of colonies with different levels of claustral investment (Figure
Simulated colony size and territory distributions matched those observed in the field, such that populations consisted of many small colonies and few large ones (
Colony and territory sizes versus reproductive investment. Because parasitic queens extend the ecological lifespan of colonies, populations that invest more in parasitic queens experience larger average colony sizes (a) and colony territory areas (b). Points show means over all simulations for a given reproductive investment, and error bars show standard deviations. In (a), all values differ (P < 0.001) except for those at 1 and 0.98 relative investment (P = 0.997); in b all values differ (P < 0.001).
Also as predicted, fire ant colonies occupied up to 12% more of the available habitat in populations that produced parasitic queens (Figure
a Percentage of available habitat occupied by fire ant colonies versus distance from the origin (bottom) of a range. Investment in parasitic queens increases and stabilizes the amount of habitat occupied by fire ant colonies b The percentage of all colonies that are headed by a parasitic queen versus distance from the origin of a range. Even small investments in parasitic queens lead to high proportions of parasitically founded colonies in the range interior. In all simulations, only claustrally founded colonies occur at the extreme range edge. Colors denote different levels of reproductive investment, lines show averages over all simulations for a given investment, and shading shows standard deviations.
The observed changes in demography and habitat occupancy were driven by the parasitic takeover of orphaned colonies. Even a slight increase in the production of parasites, from 0 to 2% of reproductive investment, led to an average of 43.1% (±20.2%) of colonies being headed by parasitic queens (Figure
Despite its positive effects on average colony size and persistence, investment in parasitic queens decreased the rate of range expansion by up to 4% (ANOVA F5, 401 = 43.593, P = 2 × 10-16, Figure
Range expansion versus reproductive investment. Investment in parasitic queens slows range expansion by diverting resources from the production of claustral queens. Points show mean maximum extents of spreading populations over all simulations for a given reproductive investment, and error bars show standard deviations. Points with different letters differ at P < 0.003.
Mature colonies occurred at an average density of 323 ±119 colonies per hectare (n = 66), which is strikingly similar to field estimates from monogyne populations in the southern USA (300 ±240 colonies/ha,
Mean reproductive investment of mature colonies from the range origin (bottom) to the top edge. Gray lines show standard deviations, dashed line shows starting average of 0.847. Populations in the saturated range interior evolve greater investment in parasitic queens, while those at the uninhabited range edge retain greater investment in dispersing claustral queens.
Range expansion is a defining character of invasive ants. In species practicing alternate life histories, range dynamics are likely affected by relative investment in different strategies. In our simulations of red imported fire ants, the production of parasitic queens resulted in larger average colony and territory sizes and higher habitat occupancy. On the other hand, by diverting investment from claustral queens that can colonize vacant habitats, the production of parasitic queens slowed range expansion. Range expansion in turn affected the fitness of colonies producing the two queen types. Colonies at expanding range edges benefitted more by investing in claustral queens that could colonize the surrounding vacant habitat, whereas those in the crowded range interior profited from investing more in parasitic queens that could take over orphaned colonies. Divergent selection regimes appeared to drive the evolution of different levels of reproductive investment based on their distance from the range edge.
The effects of range expansion also shed light on other factors shaping the evolution of reproductive strategies in ants. Parasitic founding is thought to be more beneficial in stable saturated environments, and claustral founding to be more beneficial in vacant or disturbed habitats (
Our simulated populations generally behaved realistically, highlighting the model’s value for investigating fire ant ecology. Our populations displayed near total occupancy of available habitat (
We made several simplifying assumptions in constructing our model. We assumed, for example, that habitat is constant and homogeneous and that lineages do not interbreed. Incorporating disturbance—to better capture the ecological preferences of S. invicta—would shift optimal investment toward more claustral queens by providing a steady supply of vacant habitat in which to found colonies. Allowing gene flow among lineages would slow divergence between interior and edge populations, probably shifting investment toward more claustral queens in the interior. Programing farther dispersal distances (see Appendix
The rapid spread of several invasive ant species around the globe, through multiple introduction events, provides a valuable opportunity to investigate the interplay between range expansion, dispersal, and reproduction. Because small differences in reproductive strategy cause pervasive changes in demography, habitat occupancy, range expansion, and the response to expansion-related selection, founder effects may play a major role in determining the ecological impacts of introduced ants. Subsequent selection associated with rapid range expansion may further shape the evolution of introduced populations. For similar reasons, some native ant species may be unable to shift their ranges rapidly enough to track climatic changes, and those that do may experience changes in dispersal ability or reproductive ecology as a result. In a world where ant range shifts are increasingly likely (
K. Roeder and J. Bujan provided helpful advice throughout the project. This work was funded by an OU Alumni Fellowship to JAH, and with support from the Oklahoma Biological Survey and the United States Department of Agriculture – National Institute of Food and Agriculture to ESB (NIFA-AFRI-003536).