A modeling framework for adaptive collective defense: crisis response in social-insect colonies.

Living systems, from cells to superorganismic insect colonies, have an organizational boundary between inside and outside and allocate resources to defend it. Whereas the micro-scale dynamics of cell walls can be difficult to study, the adaptive allocation of workers to defense in social-insect colonies is more conspicuous. This is particularly the case for Tetragonisca angustula stingless bees, which combine different defensive mechanisms found across other colonial animals: (1) morphological specialization (distinct soldiers (majors) are produced over weeks); (2) age-based polyethism (young majors transition to guarding tasks over days); and (3) task switching (small workers (minors) replace soldiers within minutes under crisis). To better understand how these timescales of reproduction, development, and behavior integrate to balance defensive demands with other colony needs, we developed a demographic Filippov ODE system to study the effect of these processes on task allocation and colony size. Our results show that colony size peaks at low proportions of majors, but colonies die if minors are too plastic or defensive demands are too high or if there is a high proportion of quickly developing majors. For fast maturation, increasing major production may decrease defenses. This model elucidates the demographic factors constraining collective defense regulation in social insects while also suggesting new explanations for variation in defensive allocation at smaller scales where the mechanisms underlying defensive processes are not easily observable. Moreover, our work helps to establish social insects as model organisms for understanding other systems where the transaction costs for component turnover are nontrivial, as in manufacturing systems and just-in-time supply chains.

Body mass and cuticular hydrocarbon profiles, but not queen number, underlie worker desiccation resistance in a facultatively polygynous harvester ant (Pogonomyrmex californicus).

As small-bodied terrestrial organisms, insects face severe desiccation risks in arid environments, and these risks are increasing under climate change. Here, we investigate the physiological, chemical, and behavioral mechanisms by which harvester ants, one of the most abundant arid-adapted insect groups, cope with desiccating environmental conditions. We aimed to understand how body size, cuticular hydrocarbon profiles, and queen number impact worker desiccation resistance in the facultatively polygynous harvester ant, Pogonomyrmex californicus. We measured survival at 0% humidity of field-collected worker ants sourced from three closely situated populations within a semi-arid region of southern California. These populations vary in queen number, with one population dominated by multi-queen colonies (primary polygyny), one population dominated by single-queen colonies, and one containing an even mix of single- and multi-queen colonies. We found no effect of population on worker survival in desiccation assays, suggesting that queen number does not influence colony desiccation resistance. Across populations, however, body mass and cuticular hydrocarbon profiles significantly predicted desiccation resistance. Larger-bodied workers survived longer in desiccation assays, emphasizing the importance of reduced surface area-to-volume ratios in maintaining water balance. Additionally, we observed a positive relationship between desiccation resistance and the abundance of n-alkanes, supporting previous work that has linked these high-melting point compounds to improved body water conservation. Together, these results contribute to an emerging model explaining the physiological mechanisms of desiccation resistance in insects.

Social Factors in Heat Survival: Multiqueen Desert Ant Colonies Have Higher and More Uniform Heat Tolerance.

AbstractInvestigations of thermally adaptive behavioral phenotypes are critical for both understanding climate as a selective force and predicting global species distributions under climate change conditions. Cooperative nest founding is a common strategy in harsh environments for many species and can enhance growth and competitive advantage, but whether this social strategy has direct effects on thermal tolerance was previously unknown. We examined the effects of alternative social strategies on thermal tolerance in a facultatively polygynous (multiqueen) desert ant, Pogonomyrmex californicus, asking whether and how queen number affects worker thermal tolerances. We established and reared lab colonies with one to four queens, then quantified all colony member heat tolerances (maximum critical temperature [CTmax]). Workers from colonies with more queens had higher and less variant CTmax. Our findings resemble weak link patterns, in which colony group thermal performance is improved by reducing frequencies of the most temperature-vulnerable individuals. Using ambient temperatures from our collection site, we show that multiqueen colonies have thermal tolerance distributions that enable increased midday foraging in hot desert environments. Our results suggest advantages to polygyny under climate change scenarios and raise the question of whether improved thermal tolerance is a factor that has enabled the success of polygyne species in other climatically extreme environments.

Soldier neural architecture is temporarily modality specialized but poorly predicted by repertoire size in the stingless bee Tetragonisca angustula.

Individual heterogeneity within societies provides opportunities to test hypotheses about adaptive neural investment in the context of group cooperation. Here, we explore neural investment in defense specialist soldiers of the eusocial stingless bee (Tetragonisca angustula) which are age subspecialized on distinct defense tasks and have an overall higher lifetime task repertoire than other sterile workers within the colony. Consistent with predicted behavioral demands, soldiers had higher relative visual (optic lobe) investment than nonsoldiers but only during the period when they were performing the most visually demanding defense task (hovering guarding). As soldiers aged into the less visually demanding task of standing guarding this difference disappeared. Neural investment was otherwise similar across all colony members. Despite having larger task repertoires, soldiers had similar absolute brain size and the smaller relative brain size compared to other workers, meaning that lifetime task repertoire size was a poor predictor of brain size. Both high behavioral specialization in stable environmental conditions and reassignment across task groups during a crisis occur in T. angustula. The differences in neurobiology we report here are consistent with these specialized but flexible defense strategies. This work broadens our understanding of how neurobiology mediates age and morphological task specialization in highly cooperative societies.

Complex body size differences in thermal tolerance among army ant workers (Eciton burchellii parvispinum).

In social insects, group members can differ in thermal physiology, and these differences may affect colony function. Upper thermal tolerance limits (CTmax) generally increase with body size among and within ant species, but size effects on lower thermal tolerances (CTmin) are poorly known. To test whether CTmin co-variation with body size matched patterns for CTmax, we measured CTmax and CTmin in workers of four size-based worker subcastes in the army ant Eciton burchellii parvispinum. CTmax increased with worker body size as expected. CTmin showed a more complex relationship with size: the two intermediate-size subcastes (media and porters) tolerated lower temperatures than the smallest (minims) and the largest (soldiers) worker subcastes. Body-size effects on CTmax were not predictive of body-size effects on CTmin. These patterns held for colonies collected across elevations that spanned approximately 8 °C in mean annual temperature, even though high-elevation colonies had significantly lower CTmin overall. We predict Eciton army ant subcastes will be differentially affected by directional changes in high and low temperature extremes. Worker subcastes perform distinct but complementary roles in colony function, and differential temperature effects among subcastes could impair colony performance and negatively impact colony fitness.

Extreme Insolation: Climatic Variation Shapes the Evolution of Thermal Tolerance at Multiple Scales.

The climatic variability hypothesis (CVH) is a cornerstone of thermal ecology, predicting the evolution of wider organismal thermal tolerance ranges in more thermally variable environments. Thermal tolerance ranges depend on both upper and lower tolerance limits (critical thermal maxima [[Formula: see text]] and critical thermal minima [[Formula: see text]]), which may show different responses to environmental gradients. To delineate the relative effects of mean and extreme temperatures on thermal tolerances, we conducted a within-latitude comparative test of CVH predictions for army ants (Dorylinae) at multiple scales: across elevations, in seasonal versus aseasonal forests, and in subterranean versus surface microhabitats. Consistent with the CVH, thermally buffered subterranean species had narrower thermal tolerance ranges. Both [Formula: see text] and [Formula: see text] decreased with elevation for subterranean species. In contrast, aboveground species (those exposed to insolation) showed a decrease in [Formula: see text] but no change in [Formula: see text] across elevations. Furthermore, greater seasonal temperature variation in dry forests correlated with increased [Formula: see text] but not [Formula: see text]. These patterns suggest that [Formula: see text] and [Formula: see text] respond to different abiotic selective forces: habitat-specific exposure to extreme insolation corresponds to [Formula: see text] differences but not to [Formula: see text] variation. We predict that increasingly frequent heat spikes associated with climate change will have habitat-specific physiological consequences for ectothermic animals. Models predicting climate change impacts should account for species microhabitat uses and within-latitude differences in temperature seasonality.

Weak links: how colonies counter the social costs of individual variation in thermal physiology.

Social insect nestmates often differ in thermal tolerance (the range of temperatures at which an individual functions). Worker thermal physiology can covary with body size, development, genetics and gene expression. Because colonies rely on the integration of diverse colony members, individual thermal tolerance differences can affect group performance. The weak link hypothesis states that if workers differ in thermal sensitivity, then in variable thermal environments colonies can incur performance costs due to thermal stress effects on the most thermally sensitive worker types. We discuss possible adaptive colony responses that ameliorate the costs of thermal weak links. Individual differences in thermal tolerance have profound implications for the effects of temperature variation and climate change on animal societies. Social implications of worker weak links potentially drive macroecological patterns in caste ergonomics.

Non-Nutritive Polyol Sweeteners Differ in Insecticidal Activity When Ingested by Adult Drosophila melanogaster (Diptera: Drosophilidae).

Previous work showed the non-nutritive polyol sweetener Erythritol was toxic when ingested by Drosophila melanogaster (Meigen, 1930). This study assessed whether insect toxicity is a general property of polyols. Among tested compounds, toxicity was highest for erythritol. Adult fruit flies (D. melanogaster) fed erythritol had reduced longevity relative to controls. Other polyols did not reduce longevity; the only exception was a weaker but significant reduction of female (but not male) longevity when flies were fed D-mannitol. We conclude at least some non-nutritive polyols are not toxic to adult D. melanogaster when ingested for 17 days. The longer time course (relative to erythritol) and female specificity of D-mannitol mortality suggests different mechanisms for D-mannitol and erythritol toxicity to D. melanogaster.

Microhabitat and body size effects on heat tolerance: implications for responses to climate change (army ants: Formicidae, Ecitoninae).

1. Models that predict organismal and population responses to climate change may be improved by considering ecological factors that affect species thermal tolerance. Species differences in microhabitat use can expose animals to diverse thermal selective environments at a given site and may cause sympatric species to evolve different thermal tolerances. 2. We tested the hypothesis that species differences in body size and microhabitat use (above- vs. below-ground activity) would correspond to differences in thermal tolerance (maximum critical temperatures: CTmax ). Thermal buffering effects of soil can reduce exposure to extreme high temperatures for below-ground active species. We predicted larger-bodied individuals and species would have higher CTmax and that species mean CTmax would covary positively with degree of above-ground activity. We used Neotropical army ants (Formicidae: Ecitoninae) as models. Army ants vary in microhabitat use from largely subterranean to largely above-ground active species and are highly size polymorphic. 3. We collected data on above- and below-ground temperatures in habitats used by army ants to test for microhabitat temperature differences, and we conducted CTmax assays for army ant species with varying degrees of surface activity and with different body sizes within and between species. We then tested whether microhabitat use was associated with species differences in CTmax and whether microhabitat was a better predictor of CTmax than body size for species that overlapped in size. 4. Microhabitat use was a highly significant predictor of species' upper thermal tolerance limits, both for raw data and after accounting for the effects of phylogeny. Below-ground species were more thermally sensitive, with lower maximum critical temperatures (CTmax ). The smallest workers within each species were the least heat tolerant, but the magnitude of CTmax change with body size was greater in below-ground species. Species-typical microhabitat was a stronger predictor of CTmax than body size for species that overlapped in size. Compared to the soil surface, 10-cm subsoil was a significantly moderated thermal environment for below-ground army ants, while maximum surface raid temperatures sometimes exceeded CTmax for the most thermally sensitive army ant castes. 5. We conclude sympatric species differences in thermal physiology correspond to microhabitat use. These patterns should be accounted for in models of species and community responses to thermal variation and climate change.

Erythritol, a non-nutritive sugar alcohol sweetener and the main component of truvia®, is a palatable ingested insecticide.

Insecticides have a variety of commercial applications including urban pest control, agricultural use to increase crop yields, and prevention of proliferation of insect-borne diseases. Many pesticides in current use are synthetic molecules such as organochlorine and organophosphate compounds. Some synthetic insecticides suffer drawbacks including high production costs, concern over environmental sustainability, harmful effects on human health, targeting non-intended insect species, and the evolution of resistance among insect populations. Thus, there is a large worldwide need and demand for environmentally safe and effective insecticides. Here we show that Erythritol, a non-nutritive sugar alcohol, was toxic to the fruit fly Drosophila melanogaster. Ingested erythritol decreased fruit fly longevity in a dose-dependent manner, and erythritol was ingested by flies that had free access to control (sucrose) foods in choice and CAFE studies. Erythritol was US FDA approved in 2001 and is used as a food additive in the United States. Our results demonstrate, for the first time, that erythritol may be used as a novel, environmentally sustainable and human safe approach for insect pest control.