The consequences and implications of ecology on body size distributions in social insects

The study of life history traits is central to the fields of ecology, behavior, and evolution. Life history theory explores investment into key biological characteristics that figure directly into the reproductive success and survival of an organism (e.g. size at birth, age at maturity, and size at maturity). One of the major tenets of life history theory is that finite resources must be allocated to the development of traits associated with growth, defense, and reproduction. Consequently, investment into life history traits are subject to tradeoffs between resources allocated to each demand, where resources devoted to one function can no longer be devoted to another (offspring size versus offspring number). Relative to solitary species, the study of life history traits in eusocial organisms is complicated by their reproductive division of labor. In social insects, reproduction is dominated by a queen (reproductive) caste while the majority of other tasks within the colony are performed by a worker (non-reproductive) caste, often made up of sterile individuals. The separation of reproductive and non-reproductive individuals within a colony can influence tradeoffs that constrain the evolution of life history traits in solitary organisms. For example, workers no longer invest in morphological traits required for dispersal, mating, and reproduction (with few exceptions). Additionally, in approximately 13% of ant species worker variation is large enough that the worker caste can be subdivided into sub-castes based on size and shape. For these polymorphic species, body size is both an individual and a colony-level trait (distribution of worker body sizes). Ants are typically described as most diverse and successful organisms in terrestrial ecosystems. One explanation for their ecological dominance and success is that ant species are social allowing workers to display a high degree of morphological and behavioral specialization. All of which make ants a useful system to study in order to answer a variety of questions in ecology, behavior, and evolution. Investment into worker body size and number is thought to play a major role in determining colony growth, maintenance, and reproductive output (fitness). The investment into worker body size is integral to colony fitness because it impacts most every aspect of its existence. For example, size affects worker behavior, metabolism, thermal tolerance, locomotion, longevity, and food retrieval/storage. Consequently, body size plays an important role in determining how organisms interact with the biotic and abiotic components of their environment and is often under strong selection. However, variation in size often remains pronounced within populations. In addition to its biological importance, size is also easy to measure and a common metric for a variety of research areas. Variation within and between colony investment into worker size and number may result as a response to local conditions and within evolutionary constraints. For example, within a single colony, body size and body size distributions of workers is determined by evolutionary history, genetics, the social environment within the colony, abiotic factors, nutrition, and competitive environment. Evolutionary constraints, genetics and social environment generally act “within the colony” to influence worker body size distributions. In contrast, ecological influences, which include the abiotic environment, nutrition, and competitive environment, act “outside the colony.” It is important to note that these factors do not work singly, and the interactions between factors are also important in determining body sizes within a colony. Moreover, these factors may simultaneously impact worker body size from both outside and within a colony. In the following chapters, I explore how external (ecological) factors influence body size and body size distributions in ants. I also examine how variation in worker size and number influence the outcomes of competitive interactions. I begin in Chapter One with a general review of research discussing the determinates of body size in ant species with polymorphic workers. Chapter One explores the literature examining how ecology influences body size distributions in polymorphic ant species and how variability within a colony influences measures of colony fitness. The within-colony factors influencing body size (evolutionary constraints, genetics, and social environment) have been reviewed recently, thus I keep this section brief. In the review, I discuss the intrinsic (“within a colony”) and extrinsic (“outside a colony”) determinants of intra-specific variation in ant body size. Additionally, I review the literature on how variation in worker body size can promote division of labor by increasing worker efficiency and specialization. The review focuses on species with polymorphic workers and addresses the following two questions: 1. What factors influence the distribution of worker body sizes within a colony? and 2. How does variation in body size benefit the colony? Despite considerable research in these areas, I find few studies that directly link body size variation or caste ratios to components of colony fitness. I conclude with recommendations for future work, aimed at addressing current limitations in this field. This includes a need for experimental studies that explicitly relate body size variation to fitness in social insects. In the subsequent chapters I use comparative and experimental approaches to examine the ecological factors influencing, and consequences of, variation in worker body size in polymorphic invasive ant species. Introduced species are ideal for examining the role of ecological variation on investment into worker size as they often encounter vastly different ecological conditions throughout their introduced ranges (e.g. fewer competitors and access to additional resources). These differences in ecology likely impact colony investment in growth, reproduction, and defense. Moreover, the success of invasive species is thought to occur as a result of changes to competitive environment or behavioral dominance. In this way, invasive species provide an opportunity to investigate novel species interactions that would otherwise be unethical to do experimentally if these species were intentionally introduced into new environments. In Chapter Two, I quantify the variation in size and shape of workers among geographically distinct populations of the dimorphic (two distinct worker castes) big-headed ant (Pheidole megacephala) (Fabricius). This species has been introduced nearly worldwide including areas with species rich, competitively dominant ant fauna (e.g. Australia) and to islands that have no native ants (e.g. Hawaii). I utilize this variation in ant community species richness to investigate how P. megacephala species varies investment into soldier (major) worker size, shape, and number, depending on the competitive nature of the environment. As in other dimorphic species in this genus, minor workers are behavioral “generalists” within a colony. Minor workers are significantly smaller than major workers and complete the bulk of tasks within a colony. Majors are considerably larger and more energetically costly to produce. Majors play a more specialized role in colony defense, food retrieval, and food storage. As outlined in Chapter One different ecological conditions (e.g. nutrition, food resources, abiotic environment, and competition) among populations is hypothesized to alter colony investment into worker body size. I also use genetic data to determine if the populations of P. megacephala represent cryptic species or if morphological differences are attributable to changes following introduction. I find significant variation in worker mass among five populations. Both major and minor workers were largest in Australia, whereas minor workers were smallest in Hawaii and Mauritius. I also find differences in major and minor worker morphology among populations. Majors from Mauritius have significantly larger heads (width and length) than those from Hawaii and Florida. The length of the head and tibia of minor workers are greater in South Africa compared to samples from Australia, Hawaii, and Florida. I did not find differences in caste ratios among populations. The molecular data place all samples within the same clade, supporting that these morphologically different populations represent the same species. These results suggest that the variation in shape and morphology of major and minor workers may result from a rapid adaptation or plastic response to local conditions. In Chapter Three, I examine how access to plant-based carbohydrate resources (nutrition) influences colony investment into worker body size distributions in the continuously polymorphic, red imported fire ant (Solenopsis invicta). As holometabolous insects, differences in reproductive investment and feeding prior to pupation have dramatic effects on adult ant worker body size. An increase in the total amount and quality of food resources available to a colony can increase worker size, body size distributions, and colony size. Large colonies are themselves more likely to produce larger workers, further influencing worker body size variation. Moreover, an increase in access to plant-based carbohydrate resources is suspected of playing an important role in determining invasion success of ant species as carbohydrate resources are more commonly monopolized within introduced ranges of invasive ants than in their native ranges. In this chapter, I use multiple queen (polygyne) colonies from populations in Texas, split into four treatment colonies, to experimentally test how nutrition influences colony investment into worker number, body size, body size distributions, and fat content (worker quality). Experimental colonies were reared on a diet of insect protein and one of four treatment solutions (water, amino acids, carbohydrates, and amino acid and carbohydrates). Overall, colonies with access to carbohydrates (which mimic plant based resources) produce a higher biomass of workers after 60 days. The differences in worker biomass are attributable to changes in both worker number and mean size. Worker number and size generally increases in response to carbohydrate supplementation to their diet but there is no difference in worker fat content among treatments. There is a slight shift in body size distributions (more, medium sized workers) in treatments reared on diets of carbohydrates than those denied access to carbohydrates. Invasive species with access to additional carbohydrate resources may increase colony investment into worker number and medium sized workers and subsequently influence the outcomes of competitive interactions (Chapter Four). Variation in investment into worker number and body size can influence the outcomes of competitive interactions. This includes resource discovery, food retrieval, and resource defense. There is growing interest in co-opting Lanchester’s laws, originally designed for human warfare, to predict the outcomes of aggressive interactions in ants. In Chapter Four, I use a foraging experiment and field surveys to test the predictions of Lanchester’s laws in interference competition with the continuously polymorphic, S. invicta. I also use the foraging experiment to explore how varying worker number and size influences exploitation competition. Lanchester’s square law predicts that if a group is numerically superior then attacks should occur simultaneously against their opponent and is likely most effective in open environments (or above ground). If a group is numerically inferior but possess weapons of superior “quality”, fighting in a series of one-on-one duels is more advantageous. This strategy is potentially most effective in closed and confined spaces (or below ground). I find that for colonies of equal biomass but different worker size (e.g. different worker number), colonies with smaller workers typically discover baits more quickly than those with larger workers but both large and small worker colonies retrieve equal amounts of food resources. Colonies with smaller workers do not suffer fewer losses when outnumbering their opponents than when equally matched. I however find that when colonies with large bodied workers compete with numerically dominant opponents they suffer a greater number of losses in open arenas than closed arenas (support for the square law). In closed arenas, colonies with relatively few but large workers use their size advantage in confined spaces to defend against the numerically superior but smaller workers (support for the linear law). In the field, I find more small workers above ground than below ground which supports the predictions of the linear law because in narrow confined spaces larger body size is advantageous. Lanchester’s laws provide a framework to build predictions for outcomes of competitive interactions and in the future may help identify how competition influences community structure and species composition Body size is one of the most important life history traits as it directly affects an organism’s existence. Understanding determinates of variation in ant worker body size is no trivial task. The complexity arises because of reproductive division of labor and the presence of distinct worker castes. The relative importance of factor determining worker body size within a colony varies within and among different ant species (and in some cases between worker castes). This may explain why the vast majority of research examining body size has focused on solitary organisms while relatively little work is done using social insects. Given the ecological dominance of ants in many environments however, failing to examine the factors influencing within and between colonies often limits current and future understanding of insect ecology. There is a substantial amount of information regarding the factors influencing body size in ants, but there is much left to explore.