Temnothorax Longispinosus Research Articles

Acorn ant exhibits age-dependent induced defence in response to parasitic raids.

When risk is unpredictable, organisms may evolve induced defenses, which are activated after an indication of increased risk. In colonies with behavioural specialization, investment in defence may not be uniformly beneficial among group members. Instead, it should depend on the individual's likelihood of participating in defence. The ant Temnothorax longispinosus uses venom to defend against raids by the social parasite Temnothorax americanus. We tested whether T. longispinosus upregulate investment in venom after experiencing a raid, investigating the relationship between venom volume and worker behavioural caste. Overall, raided colonies had more venom per capita than unraided colonies. When divided into behavioural castes, foragers had more venom after experiencing a raid, while nurses did not. These results demonstrate that T. longispinosus have an induced chemical defence against parasitic raids. However, instead of this defence being deployed uniformly among all workers, the induction of the defence depends on the behavioural caste, and therefore age, of the worker, implying that plasticity in venom production increases with age. Since older social insect workers tend to perform riskier tasks, inducibility may align with an increase in expected risk of death, especially if foragers are more likely to defend the colony against parasites than younger workers.

Genomic basis of adaptation to climate and parasite prevalence and the importance of odorant perception in the ant Temnothorax longispinosus.

A co-evolutionary arms race ensues when parasites exhibit exploitative behaviour, which prompts adaptations in their hosts, in turn triggering counter-adaptations by the parasites. To unravel the genomic basis of this coevolution from the host's perspective, we collected ants of the host species Temnothorax longispinosus, parasitized by the social parasite Temnothorax americanus, from 10 populations in the northeastern United States exhibiting varying levels of parasite prevalence and living under different climatic conditions. We conducted a genome-wide association study (GWAS) to identify single nucleotide polymorphisms (SNPs) associated with both prevalence and climate. Our investigation highlighted a multitude of candidate SNPs associated with parasite prevalence, particularly in genes responsible for sensory perception of smell including odorant receptor genes. We further focused on population-specific compositions of cuticular hydrocarbons, a complex trait important for signalling, communication and protection against desiccation. The relative abundances of n-alkanes were correlated with climate, while there was only a trend between parasite prevalence and the relative abundances of known recognition cues. Furthermore, we identified candidate genes likely involved in the synthesis and recognition of specific hydrocarbons. In addition, we analysed the population-level gene expression in the antennae, the primary organ for odorant reception, and established a strong correlation with parasite prevalence. Our comprehensive study highlights the intricate genomic patterns forged by the interplay of diverse selection factors and how these are manifested in the expression of various phenotypes.

Temnothorax longispinosus acorn ant colonies respond to parasitic raids by emigrating

Temnothorax longispinosus acorn ant colonies respond to parasitic raids by emigrating

The effect of urbanization and temperature on thermal tolerance, foraging performance, and competition in cavity-dwelling ants.

Human disturbance including rapid urbanization and increased temperatures can have profound effects on the ecology of local populations. Eusocial insects, such as ants, have adapted to stressors of increasing temperature and urbanization; however, these evolutionary responses are not consistent among populations across geographic space. Here we asked how urbanization and incubation temperature influence critical thermal maximum (CTmax) and various ecologically relevant behaviors in three ant species in urban and rural locations in Worcester, MA, USA. We did this by incubating colonies of three species of cavity dwelling ant (Aphaenogaster picea, Tapinoma sessile, and Temnothorax longispinosus) from 2 habitat types (Rural and Urban), for 60-days at multiple temperatures. We found that incubation temperature, urbanization, and species of ant all significantly affected overall colony critical thermal maximum. We also found that recruitment time, colonization time, and defense response were significantly affected by incubation temperature and varied between species of ant, while recruitment and colonization time were additionally affected by urbanization. These variable changes in performance and competitive traits across species suggest that responses to urbanization and shifting temperatures are not universal across species. Changes in behavioral responses caused by urbanization may disrupt biodiversity, creating unusual competitive environments as a consequence of natural adaptations and cause both direct and indirect mechanisms for which human disturbance can lead to local species extinction.

Testing optimal defence theory in a social insect: Increased risk is correlated with increased venom investment

Abstract Investment in defence may not be uniformly beneficial across an organism's lifespan. Risk, and therefore potential payoff of defence, may change with age and behaviour, but for colony‐living organisms, it may also change with colony size and reproductive stage. The acorn ant Temnothorax longispinosus uses venom to defend against socially parasitic ants that raid their nests to steal brood. We investigated the idea that T. longispinosus adjust their venom allocation in accordance with raid risk. We tested the predictions that T. longispinosus ants should produce more venom when raids are most likely to occur and during the parts of the nest reproductive cycle when the potential fitness loss per raid is highest. We also asked whether venom volume varies between nurses and foragers within a colony, which have different potential risk levels, and whether this difference increases with colony size. We found that workers had more venom in the summer, both before and during the period when raids occur, than in the fall when pupae were no longer present in nests. Workers engaging in nursing behaviours had more venom as the pupa to worker ratio in the nest increased, indicating that nurses invest more in venom as the relative number of pupae requiring defence increases. In addition, the difference in venom volume between nurses and foragers grew with colony size. These results provide observational support for the hypothesis that individuals vary their investment in venom over their colony's development in conjunction with the risk of social parasitism.

Task-specific odorant receptor expression in worker antennae indicates that sensory filters regulate division of labor in ants

Division of labor (DOL) is a characteristic trait of insect societies, where tasks are generally performed by specialized individuals. Inside workers focus on brood or nest care, while others take risks by foraging outside. Theory proposes that workers have different thresholds to perform certain tasks when confronted with task-related stimuli, leading to specialization and consequently DOL. Workers are presumed to vary in their response to task-related cues rather than in how they perceive such information. Here, we test the hypothesis that DOL instead stems from workers varying in their efficiency to detect stimuli of specific tasks. We use transcriptomics to measure mRNA expression levels in the antennae and brain of nurses and foragers of the ant Temnothorax longispinosus. We find seven times as many genes to be differentially expressed between behavioral phenotypes in the antennae compared to the brain. Moreover, half of all odorant receptors are differentially expressed, with an overrepresentation of the 9-exon gene family upregulated in the antennae of nurses. Nurses and foragers thus apparently differ in the perception of their olfactory environment and task-related signals. Our study supports the hypothesis that antennal sensory filters predispose workers to specialize in specific tasks.

Histone acetyltransferases and external demands influence task switching in Temnothorax ants.

In social hymenopterans, workers specialize in different tasks. Whether a worker nurses the brood or forages is influenced by the responsiveness for task-related cues which in turn is determined by gene expression. Task choice is dynamic and changes throughout a worker's life, e.g. with age or in response to increased demands for certain tasks. Behavioural switches require the ability to adjust gene expression but the mechanisms regulating such transcriptional adaptations remain elusive. We investigated the role of histone acetylation in task specialization and behavioural flexibility in Temnothorax longispinosus ants. By inhibiting p300/CBP histone acetyltransferases (HAT) and manipulating colony composition, we found that HAT inhibition impairs the ability of older workers to switch to brood care. Yet, HAT inhibition increased the ability of young workers to accelerate their behavioural development and switch to foraging. Our data suggest that HAT in combination with social signals indicating task demands play an important role in modulating behaviour. Elevated HAT activity may contribute to keeping young brood carers from leaving the nest, where they would be exposed to high mortality. These findings shed light on the epigenetic processes underlying behavioural flexibility in animals and provide insight into the mechanisms of task specialization in social insects.

Comparative analyses of caste, sex, and developmental stage-specific transcriptomes in two Temnothorax ants.

Social insects dominate arthropod communities worldwide due to cooperation and division of labor in their societies. This, however, makes them vulnerable to exploitation by social parasites, such as slave‐making ants. Slave‐making ant workers pillage brood from neighboring nests of related host ant species. After emergence, host workers take over all nonreproductive colony tasks, whereas slavemakers have lost the ability to care for themselves and their offspring. Here, we compared transcriptomes of different developmental stages (larvae, pupae, and adults), castes (queens and workers), and sexes of two related ant species, the slavemaker Temnothorax americanus and its host Temnothorax longispinosus. Our aim was to investigate commonalities and differences in group‐specific transcriptomes, whereupon across‐species differences possibly can be explained by their divergent lifestyles. Larvae and pupae showed the highest similarity between the two species and upregulated genes with enriched functions of translation and chitin metabolism, respectively. Workers commonly upregulated oxidation‐reduction genes, possibly indicative of their active lifestyle. Host workers, but not workers of the slavemaker, upregulated a “social behavior” gene. In slavemaker queens and workers, genes associated with the regulation of transposable elements were upregulated. Queens of both species showed transcriptomic signals of anti‐aging mechanisms, with hosts upregulating various DNA repair pathways and slavemaker queens investing in trehalose metabolism. The transcriptomes of males showed enriched functions for quite general terms realized in different genes and pathways in each species. In summary, the strong interspecific commonalities in larvae, pupae, and workers were reflected in the same enriched Gene Ontology (GO) terms. Less commonalities occurred in the transcriptomes of queens and males, which apparently utilize different pathways to achieve a long life and sperm production, respectively. We found that all analyzed groups in this study show characteristic GO terms, with similar patterns in both species.

A Role of Histone Acetylation in the Regulation of Circadian Rhythm in Ants.

SummaryIn many organisms, circadian rhythms and associated oscillations in gene expression are controlled by post-translational modifications of histone proteins. Although epigenetic mechanisms influence key aspects of insect societies, their implication in regulating circadian rhythms has not been studied in social insects. Here we ask whether histone acetylation plays a role in adjusting circadian activity in the ant Temnothorax longispinosus. We characterized activity patterns in 20 colonies to reveal that these ants exhibit a diurnal rhythm in colony-level activity and can rapidly respond to changes in the light regime. Then we fed T. longispinosus colonies with C646, a chemical inhibitor of histone acetyltransferases, to show that treated colonies lost their circadian rhythmicity and failed to adjust their activity to the light regime. These findings suggest a role for histone acetylation in controlling rhythmicity in ants and implicate epigenetic processes in the regulation of circadian rhythms in a social context.

A Role of Histone Acetylation in the Regulation of Circadian Rhythm in Ants

Circadian rhythms and associated oscillating gene expression patterns are controlled in many organisms by post-translational modifications of histone proteins. Although epigenetic mechanisms have been suggested to influence key aspects of insect societies, the role of histone modifications in regulating their circadian rhythm has never been studied. Here we ask whether histone acetylation plays a role in adjusting the circadian rhythm in colonies of the ant Temnothorax longispinosus. First, we characterized the circadian activity of 20 colonies by recording the proportion of active ants inside and outside the nest every hour over four days under a 12h:12h light:dark regime. Our analyses revealed that T. longispinosus ants are diurnal and show a clear circadian rhythm in colony-level activity. Second, we tested circadian rhythmicity after shifting the light regime six hours forward to find that the peak activity also moved six hours forward, revealing that colonies rapidly adjust to changes in the light regime. Finally, we investigated whether histone acetylation regulates rhythmicity and its adjustment to light by feeding T. longispinosus colonies with C646, a chemical inhibitor of histone acetyltransferases. Treated colonies lost their circadian rhythmicity, and failed to adjust their activity to the new light regime. These findings suggest a role for histone acetylation in underlying rhythmicity and synchronization of the periodic activity to external cues in T. longispinosus, and implicate epigenetic processes in the regulation of circadian rhythm in a social context.

Ant personalities and behavioral plasticity along a climatic gradient

Variable environments can select for behavioral plasticity. Yet, along environmental gradients, personalities (consistent differences in behavior) and behavioral syndromes (associations between behavioral traits) can arise both across and within populations, which point to limits in behavioral plasticity. To date, little is known on how behavioral plasticity and animal personalities are associated along geographical gradients. Hereto, we subjected colonies of the ant Temnothorax longispinosus from populations along a natural climatic gradient to temperature manipulations and behavioral experiments. We asked whether personalities and behavioral syndromes stem from local adaptations or are plastic responses and whether the extent of behavioral plasticity differs between populations from warmer versus colder habitats. Our results reveal that colonies responded to warmer temperatures with increased explorative and brood care behavior. Interestingly, these behavioral traits shifted in the same direction as a syndrome previously found along this climatic gradient, where colonies from warmer environments displayed more exploration and brood care. Additionally, colonies that exhibited lower aggression but more exploration prior to temperature manipulations showed the highest behavioral plasticity. Moreover, only in one behavioral trait, exploration, colonies from colder sites exhibited higher plasticity than those from warmer sites. This suggests that ant behaviors are influenced mostly by prevailing conditions with a limited influence of past experience on behavioral plasticity. Our study proposes that associations between behavioral traits can be modified by climatic conditions, thus providing insights into the complex ways animals respond to current and past environments. Behavioral plasticity and animal personalities could be linked to climate. Yet few studies have investigated behavioral associations along geographical gradients. Hence, we still lack an understanding of how current and past environmental conditions affect such behavioral associations along gradients. Here, we asked whether the extent of behavioral plasticity differs between populations from warmer versus colder sites along a climatic gradient and whether animal personalities stem from local adaptations or plastic responses. We demonstrate in a social insect that associations between behavioral traits can be modified by temperature. Specifically, in response to temperature changes, behavioral traits shifted in a direction consistent with variation in a syndrome across a climatic gradient. This study provides unique empirical support linking animal personalities and phenotypic plasticity across populations along climatic gradients, thus offering new insights into the complex ways animals respond to current conditions and past experience.

Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite.

The geographical mosaic theory of coevolution predicts that species interactions vary between locales. Depending on who leads the coevolutionary arms race, the effectivity of parasite attack or host defence strategies will explain parasite prevalence. Here, we compare behaviour and brain transcriptomes of Temnothorax longispinosus ant workers when defending their nest against an invading social parasite, the slavemaking ant Temnothorax americanus. A full-factorial design allowed us to test whether behaviour and gene expression are linked to parasite pressure on host populations or to the ecological success of parasite populations. Albeit host defences had been shown before to covary with local parasite pressure, we found parasite success to be much more important. Our chemical and behavioural analyses revealed that parasites from high prevalence sites carry lower concentrations of recognition cues and are less often attacked by hosts. This link was further supported by gene expression analysis. Our study reveals that host-parasite interactions are strongly influenced by social parasite strategies, so that variation in parasite prevalence is determined by parasite traits rather than the efficacy of host defence. Gene functions associated with parasite success indicated strong neuronal responses in hosts, including long-term changes in gene regulation, indicating an enduring impact of parasites on host behaviour. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Gene expression is more strongly associated with behavioural specialization than with age or fertility in ant workers.

The ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and more corpulent. Here, we experimentally disentangle behavioural specialization from age and fertility inTemnothorax longispinosus ant workers and analyse how these parameters are linked to whole-body gene expression. A total of 3,644 genes were associated with behavioural specialization which is ten times more than associated with age and 50 times more than associated with fertility. Brood carers were characterized by an upregulation of three Vitellogenin (Vg) genes, one of which, Vg-like A, was the most differentially expressed gene that was recently shown experimentally to control the switch from brood to worker care. The expression of Conventional Vg was unlinked to behavioural specialization, age or fertility, which contrasts to studies on bees and some ants. Diversity in Vg/Vg-like copy number and expression bias across ants supports subfunctionalization of Vg genes and indicates that some regulatory mechanisms of division of labour diverged in different ant lineages. Simulations revealed that our experimental dissociation of co-varying factors reduced transcriptomic noise, suggesting that confounding factors could potentially explain inconsistencies across transcriptomic studies of behavioural specialization in ants. Thus, our study reveals that worker gene expression is mainly linked to the worker's function for the colony and provides novel insights into the evolution of sociality in ants.

Combat, co-existence, and resource partitioning in acorn-dwelling Temnothorax ants

Coexisting populations of ecologically similar species may reduce competition by decreasing overlap in the resources they use, or by spatially or temporally partitioning shared resources. Temnothorax longispinosus and Temnothorax curvispinosus are morphologically similar acorn-nesting ant species that frequently co-occur in the leaf litter of deciduous forests of eastern North America. By conducting two detailed and complementary field surveys, we show that T. longispinosus and T. curvispinosus nest in a specialized subset of available acorns and that nests had a uniform pattern of spacing consistent with spatial displacement from competition. Colonies of both species were then subjected to laboratory preference tests, and interspecific and intraspecific competition experiments. The preference experiments demonstrated some level of differentiation in resource use among species within the specialized range of nest properties used by the ants in nature, potentially reducing competition during nest selection. Nevertheless, in both intraspecific competition experiments we found high mortality that increased when ants were initially in nests closer together. T. curvispinosus mortality also increased with the number of combatants, consistent with a battle of attrition between opposing sides. In contrast, T. longispinosus mortality decreased during battles as the number of combatants increased. In the interspecific battles, both T. curvispinosus and T. longispinosus sustained some mortality, but escalated battles did not occur. Broadly, this work demonstrates that direct competition over nesting sites is an important mechanism underlying the dispersion of Temnothorax nests and therefore the structuring of acorn-nesting Temnothorax assemblages.

A List of Ants (Hymenoptera: Formicidae) Collected During the 2017 William H. Cross Expedition to the Ouachita Mountains of Arkansas with New State Records

ABSTRACT The William H. Cross Expedition is an endowed collecting trip conducted annually by the Mississippi Entomological Museum. This year's expedition was held from 19 to 24 June 2017 at the Ouachita Mountains Biological Station (OMBS) in Polk County, Arkansas. We focused our collecting efforts on the mountainous Ouachita Mountains Biological Station, but we also collected at various sites within the Ouachita National Forest, at Queen Wilhelmina State Park, Big Fork Creek Natural Area, and Stone Road Glade Natural Area. During a five-day period, we collected 63 ant species, including five not previously reported for Arkansas: Brachyponera chinensis (Emery), Hypoponera inexorata (Wheeler), Strumigenys creightoni Smith, Syscia augustae Wheeler, and Temnothorax longispinosus (Roger).

Intrinsic worker mortality depends on behavioral caste and the queens' presence in a social insect.

According to the classic life history theory, selection for longevity depends on age-dependant extrinsic mortality and fecundity. In social insects, the common life history trade-off between fecundity and longevity appears to be reversed, as the most fecund individual, the queen, often exceeds workers in lifespan several fold. But does fecundity directly affect intrinsic mortality also in social insect workers? And what is the effect of task on worker mortality? Here, we studied how social environment and behavioral caste affect intrinsic mortality of ant workers. We compared worker survival between queenless and queenright Temnothorax longispinosus nests and demonstrate that workers survive longer under the queens' absence. Temnothorax ant workers fight over reproduction when the queen is absent and dominant workers lay eggs. Worker fertility might therefore increase lifespan, possibly due to a positive physiological link between fecundity and longevity, or better care for fertile workers. In social insects, division of labor among workers is age-dependant with young workers caring for the brood and old ones going out to forage. We therefore expected nurses to survive longer than foragers, which is what we found. Surprisingly, inactive inside workers showed a lower survival than nurses but comparable to that of foragers. The reduced longevity of inactive workers could be due to them being older than the nurses, or due to a positive effect of activity on lifespan. Overall, our study points to behavioral caste-dependent intrinsic mortality rates and a positive association between fertility and longevity not only in queens but also in ant workers.

The influence of space and time on the evolution of altruistic defence: the case of ant slave rebellion.

How can antiparasite defence traits evolve even if they do not directly benefit their carriers? An example of such an indirect defence is rebellion of enslaved Temnothorax longispinosus ant workers against their social parasite Temnothorax americanus, a slavemaking ant. Ant slaves have been observed to kill their oppressors' offspring, a behaviour from which the sterile slaves cannot profit directly. Parasite brood killing could, however, reduce raiding pressure on related host colonies nearby. We analyse with extensive computer simulations for the Temnothorax slavemaker system under what conditions a hypothetical rebel allele could invade a host population, and in particular, how host-parasite dynamics and population structure influence the rebel allele's success. Exploring a wide range of model parameters, we only found a small number of parameter combinations for which kin selection or multilevel selection could allow a slave rebellion allele to spread in the host population. Furthermore, we did not detect any cases in which the reduction of raiding pressure in the close vicinity of the slavemaker nest would substantially contribute to the inclusive fitness of rebels. This suggests that slave rebellion is not costly and perhaps a side-effect of some other beneficial trait. In some of our simulations, however, even a costly rebellion allele could spread in the population. This was possible when host-parasite interactions led to a metapopulation dynamic with frequent local extinctions and recolonizations of demes by the offspring of few immigrants.

Intraspecific variation in collective behaviors drives interspecific contests in acorn ants

Intraspecific variation in behavior has largely been neglected by community ecologists to date. Recently, however, a number of studies demonstrated that intraspecific variation can have profound consequences for species interactions and thereby alter community dynamics in solitary organisms. Here, we study how intraspecific variation in behaviors (also called collective personalities) affects the outcome of resource contests between 2 co-occurring species of ants, Temnothorax longispinosus and T. curvispinosus. Our results revealed that intraspecific variation in colonies’ exploration behavior and aggressiveness predicts the outcome of interspecific contests for food and nest sites. How exploratory behavior affected the outcome of the foraging and nest site contests depended on the species: exploratory behavior seemed to enhance performance in foraging contests in T. curvispinosus but diminish it in T. longispinosus. More interestingly, whether a species was successful in nest site contests depended not only on its personality but also on the personality of its opponent colony. Temnothorax longispinosus experienced greater success if its opponent colony had similar exploratory tendencies to its own. In contrast, T. curvispinosus performed best when its opponent colony exhibited a contrasting exploratory tendency to its own. Our data demonstrate that intraspecific variation in colony behavior can have consequences for contest outcomes and ensure that no one species or behavioral strategy consistently experiences superior success. This, in turn, might help to maintain variation in behavior in multiple interacting populations and prevent competitive exclusion of one of the species.

Ant recognition cue diversity is higher in the presence of slavemaker ants

Social insect colonies defend themselves from intruders through nestmate recognition, yet the evolution and maintenance of recognition cue diversity is still poorly understood. We compared the recognition cue diversity of 9 populations of Temnothorax longispinosus ant colonies, including populations that harbored the socially parasitic slavemaker ant, Protomognathus americanus. Although ants recognize friends from foe based on recognition cues encoded in their cuticular hydrocarbon profile, which specific compounds are involved in recognition is unknown for most species. We therefore started by statistically identifying 9 putative recognition compounds involved in worker and colony aggression. We find that colonies that co-occur with slavemakers were more variable in these recognition compounds and hence less similar in their recognition profiles than unparasitized populations. Importantly, these differences appear to be regulated by processes that specifically act on the level of the colony, which rules out potentially confounding effects altering chemical profiles of populations, such as differences in abiotic conditions or standing genetic variation. Instead, our findings indicate that slavemakers drive recognition cue diversity in their ant hosts, in much the same way that avian hosts diversify their egg appearance in response to brood parasite pressure. Such recognition cue diversification through negative frequency-dependent selection favors rare host phenotypes and renders it impossible for parasites to match the recognition profile of all potential hosts.

The ecological success of a social parasite increases with manipulation of collective host behaviour.

Many parasites alter the behaviour of their host to their own advantage, yet hosts often vary in their susceptibility to manipulation. The ecological and evolutionary implications of such variation can be profound, as resistant host populations may suffer lower parasite pressures than those susceptible to manipulation. To test this prediction, we assessed parasite-induced aggressive behaviours across 16 populations of two Temnothorax ant species, many of which harbour the slavemaker ant Protomognathus americanus. This social parasite uses its Dufour's gland secretions to manipulate its hosts into attacking nestmates, which may deter defenders away from itself during invasion. We indeed find that colonies that were manipulated into attacking their Dufour-treated nestmates were less aggressive towards the slavemaker than those that did not show slavemaker-induced nestmate attack. Slavemakers benefited from altering their hosts' aggression, as both the likelihood that slavemakers survived host encounters and slavemaker prevalence in ant communities increased with slavemaker-induced nestmate attack. Finally, we show that Temnothorax longispinosus colonies were more susceptible to manipulation than Temnothorax curvispinosus colonies. This explains why T.curvispinosus colonies responded with more aggression towards invading slavemakers, why they were less likely to let slavemakers escape and why they were less frequently parasitized by the slavemaker than T.longispinosus. Our findings highlight that large-scale geographic variation in resistance to manipulation can have important implications for the prevalence and host preference of parasites.