Causes and Consequences of Intraspecific Variation in Behavior of the Red Imported Fire Ant

Organisms vary at the individual and population level in many ecologically relevant traits. This study documents and quantifies colony-level variation in ecologically important behaviors of a widespread invasive social insect, demonstrates multitrophic ecological effects of this colony-level variation, and explores genetic factors that may affect and predict behavior at the colony-level. I quantified significant, persistent regional and colony-level variation in the red imported fire ant (Solenopsis invicta) in behaviors such as extra-nest activity, exploration, and resource discovery speed and recruitment effort. Colony behavior correlated with both colony productivity and colony growth. Using single-lineage colonies, I estimated broad-sense heritability of between 0.45 and 0.5 for the observed colony behaviors. I created experimental microcosms comprised of fire ant colonies, plants, and insect herbivores. Differences in fire ant colony behavior linked to carbohydrate attraction directly impacted herbivore mortality and indirectly impacted plant damage. I quantified colony differences colony differences in the expression of the fire ant foraging gene (sifor) as well as colony-level differences in behavior for fire ant colonies collected from across a large area of Texas. Expression of sifor was more than three-fold higher in fire ant foragers than in fire ant workers in the interior of the nest, and colony-level differences in sifor expression of foragers and interior workers correlated with colony behavior. Higher sifor expression in foragers correlated with higher foraging activity, exploratory activity, and recruitment to nectar in fire ant colonies. Finally, I explored the hypothesis that fire ant foundress groups could maximize inclusive fitness benefits and alter cooperative and competitive behaviors in response to cues indicating higher relatedness of foundresses. I found that group and queen performance was significantly affected by group composition. Groups composed of foundresses that were less likely to be related produced no more workers than queens founding alone, while groups composed of foundresses from the same site produced the most workers of all group types. The conclusions of this study have widespread implications for many social insects and their ecological interactions. By further exploring these effects at the mechanistic, organismal, and ecological level we will improve our understanding of collective behavior, social evolution, and intraspecific variation

Data from: Intraspecific variation among social insect colonies: persistent regional and colony-level differences in fire ant foraging behavior

Individuals vary within a species in many ecologically important ways, but the causes and consequences of such variation are often poorly understood. Foraging behavior is among the most profitable and risky activities in which organisms engage and is expected to be under strong selection. Among social insects there is evidence that within-colony variation in traits such as foraging behavior can increase colony fitness, but variation between colonies and the potential consequences of such variation are poorly documented. In this study, we tested natural populations of the red imported fire ant, Solenopsis invicta, for the existence of colony and regional variation in foraging behavior and tested the persistence of this variation over time and across foraging habitats. We also reared single-lineage colonies in standardized environments to explore the contribution of colony lineage. Fire ants from natural populations exhibited significant and persistent colony and regional-level variation in foraging behaviors such as extra-nest activity, exploration, and discovery of and recruitment to resources. Moreover, colony-level variation in extra-nest activity was significantly correlated with colony growth, suggesting that this variation has fitness consequences. Lineage of the colony had a significant effect on extra-nest activity and exploratory activity and explained approximately half of the variation observed in foraging behaviors, suggesting a heritable component to colony-level variation in behavior

Data from: Colony-level behavioral variation correlates with differences in expression of the foraging gene in red imported fire ants

Among social insects, colony-level variation is likely to be widespread and have significant ecological consequences. Very few studies, however, have documented how genetic factors relate to behavior at the colony level. Differences in expression of the foraging gene have been associated with differences in foraging and activity of a wide variety of organisms. We quantified expression of the red imported fire ant foraging gene (sifor) in workers from 21 colonies collected across the natural range of Texas fire ant populations, but maintained under standardized, environmentally controlled conditions. Colonies varied significantly in their behavior. The most active colonies had up to 10 times more active foragers than the least active colony and more than 16 times as many workers outside the nest. Expression differences among colonies correlated with this colony-level behavioral variation. Colonies with higher sifor expression in foragers had, on average, significantly higher foraging activity, exploratory activity, and recruitment to nectar than colonies with lower expression. Expression of sifor was also strongly correlated with worker task (foraging versus working in the interior of the nest). These results provide insight into the genetic and physiological processes underlying collective differences in social behavior. Quantifying variation in expression of the foraging gene may provide an important tool for understanding and predicting the ecological consequences of colony-level behavioral variation

Intraspecific Variation among Social Insect Colonies: Persistent Regional and Colony-Level Differences in Fire Ant Foraging Behavior

<div><p>Individuals vary within a species in many ecologically important ways, but the causes and consequences of such variation are often poorly understood. Foraging behavior is among the most profitable and risky activities in which organisms engage and is expected to be under strong selection. Among social insects there is evidence that within-colony variation in traits such as foraging behavior can increase colony fitness, but variation between colonies and the potential consequences of such variation are poorly documented. In this study, we tested natural populations of the red imported fire ant, <i>Solenopsis invicta</i>, for the existence of colony and regional variation in foraging behavior and tested the persistence of this variation over time and across foraging habitats. We also reared single-lineage colonies in standardized environments to explore the contribution of colony lineage. Fire ants from natural populations exhibited significant and persistent colony and regional-level variation in foraging behaviors such as extra-nest activity, exploration, and discovery of and recruitment to resources. Moreover, colony-level variation in extra-nest activity was significantly correlated with colony growth, suggesting that this variation has fitness consequences. Lineage of the colony had a significant effect on extra-nest activity and exploratory activity and explained approximately half of the variation observed in foraging behaviors, suggesting a heritable component to colony-level variation in behavior.</p></div

Colony and regional variation in fire ant foraging behavior before and after exposure to different foraging habitats

Raw data for analysis of regional and colony-level variation in fire ant foraging behavior. Data includes fire ant foraging behavior before and after five weeks exposure to ground-level vs. elevated foraging habitat types. Recruitment to ground-level and elevated resources, disovery and trail formation times, extra-nest activity, and exploratory activity are included, as well as weight of food collected and final colony size

Colony differences in fire ant foraging behavior before and after exposure to different foraging habitats.

<p>Graphs show average number of ants (A) at a ground-level cricket, (B) at a cricket elevated 30cm up a wooden dowel, (C) active outside the nest and (D) exploring a novel structure. Each line represents average for a colony of origin (n = 2), for fire ant colonies from Texas (left) and Mississippi (right) before and after five weeks exposure to different foraging habitat treatments.</p

Average number of fire ants recruiting to ground-level or elevated crickets.

<p>Crickets were placed at (A) ground-level or (B) 30cm up a wooden dowel, prior to experimental treatment. Each bar represents average recruitment for a single colony of origin (n = 2); error bars show standard error.</p

Regional differences in recruitment of fire ants to ground-level or elevated crickets.

<p>Colonies were collected in Texas (light diamond, n = 17) or Mississippi (dark square, n = 16) and crickets were placed at ground-level (A and B) or 30cm up a wooden dowel (C and D). (A) and (C) show average number of ants observed at the cricket over time while (B) and (D) show the average time to resource discovery and time to formation of a recruiting trail. Error bars show standard error.</p

Effects of behavior on fire ant colony performance measures.

<p>Graphs show (A) Ground-level recruitment versus colony food collection and (B) extra-nest activity versus colony size (final dry weight of workers and brood).</p

What Goes Up Might Come Down: the Spectacular Spread of an Endosymbiont Is Followed by Its Decline a Decade Later

Facultative, intracellular bacterial symbionts of arthropods may dramatically affect host biology and reproduction. The length of these symbiont-host associations may be thousands to millions of years, and while symbiont loss is predicted, there have been very few observations of a decline of symbiont infection rates. In a population of the sweet potato whitefly species (Bemisia tabaci MEAM1) in Arizona, USA, we documented the frequency decline of a strain of Rickettsia in the Rickettsia bellii clade from near-fixation in 2011 to 36% of whiteflies infected in 2017. In previous studies, Rickettsia had been shown to increase from 1 to 97% from 2000 to 2006 and remained at high frequency for at least five years. At that time, Rickettsia infection was associated with both fitness benefits and female bias. In the current study, we established matrilines of whiteflies from the field (2016, Rickettsia infection frequency = 58%) and studied (a) Rickettsia vertical transmission, (b) fitness and sex ratios associated with Rickettsia infection, (c) symbiont titer, and (d) bacterial communities within whiteflies. The vertical transmission rate was high, approximately 98%. Rickettsia infection in the matrilines was not associated with fitness benefits or sex ratio bias and appeared to be slightly costly, as more Rickettsia-infected individuals produced non-hatching eggs. Overall, the titer of Rickettsia in the matrilines was lower in 2016 than in the whiteflies collected in 2011, but the titer distribution appeared bimodal, with high- and low-titer lines, and constancy of the average titer within lines over three generations. We found neither association between Rickettsia titer and fitness benefits or sex ratio bias nor evidence that Rickettsia was replaced by another secondary symbiont. The change in the interaction between symbiont and host in 2016 whiteflies may explain the drop in symbiont frequency we observed.12 month embargo; published online: 12 August 2019This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]