Ant Temnothorax Nylanderi Research Articles

Limited contamination by trace metals in city colonies of the ant Temnothorax nylanderi (Foerster, 1850)

Limited contamination by trace metals in city colonies of the ant Temnothorax nylanderi (Foerster, 1850)

The influence of parasite load on transcriptional activity and morphology of a cestode and its ant intermediate host.

Parasites with complex life cycles are known to induce phenotypic changes in their intermediate hosts to increase transmission to the final host. The magnitude of these changes could increase with the number of parasites, which would be beneficial to co-infecting parasites. Yet, adverse effects of high parasite load (i.e. many parasites in a single host) might stress both hosts and parasites (e.g. through an increased immune response). We investigated the consequences of parasite load on the transcriptional activity and morphology of the cestode Anomotaenia brevis and its intermediate host, the ant Temnothorax nylanderi. We demonstrated that many differentially expressed host genes shifted with parasite load, and their functions indicate a stronger immune response and fight against oxidative stress in heavily infected hosts. The expression of other host genes responded to infection in an all-or-nothing manner, as did the morphology of the host workers. However, the cestodes became smaller when they competed with other parasites for resources from a single host. Their expression profile further indicated shifts in host immune avoidance, starvation resistance and vesicle-mediated transport. In summary, our study reveals clear consequences of parasite load and highlights specific processes and traits affected by this.

Urban colonies are less aggressive but forage more than their forest counterparts in the ant Temnothorax nylanderi

Urban colonies are less aggressive but forage more than their forest counterparts in the ant Temnothorax nylanderi

Spring colonies of the ant Temnothorax nylanderi tolerate cadmium better than winter colonies, in both a city and a forest habitat.

A recent study showed that, in the ant Temnothorax nylanderi, city colonies are more tolerant to cadmium than forest colonies. However, because of annual variation in biological factors (e.g. body size, anti-stress protein production or trace metal accumulation rate), trace metal tolerance may vary over the year. We aimed at testing whether tolerance to cadmium of colonies of T. nylanderi differs between two different seasons within the same year (winter and spring). We also assessed whether the better cadmium tolerance of city colonies was constant over these two different time points. We collected colonies at the end of their hibernation period (winter colonies) and several weeks after (spring colonies) from two different habitats (forest and city) to assess whether response to cadmium was consistent regardless of the environment. We exposed colonies to a cadmium or a control treatment for 61 days. We compared tolerance to cadmium between spring/winter and city/forest colonies by measuring several life history traits. We found that spring colonies tolerates cadmium better than winter colonies, and that city colonies have a higher tolerance to cadmium but only in spring. Although further studies with replicated pairs of city/forest habitats and different years will be necessary to confirm those results, our study suggests that tolerance to trace metals can fluctuate along the yearly cycle.

Disentangling the roles of social and individual effects on cadmium tolerance in the ant Temnothorax nylanderi

Abstract Urbanization brings new pressures for individuals. Among them, trace elements, such as cadmium, are important stressors. A recent study highlights a weaker negative effect of cadmium on city colonies relative to their forest counterparts in the ant Temnothorax nylanderi. Here, we aim to test whether the better tolerance of city colonies in this species results from a better ability of workers to rear larvae despite stressful conditions and/or a better ability of larvae to develop properly despite stressful conditions. We performed a cross-fostering experiment of workers and larvae from city and forest colonies, in common garden conditions in the laboratory. Colonies were fed using cadmium-enriched or cadmium-free food for 2 months, and we measured four life-history traits. As expected, cadmium had a negative impact on all traits. Unexpectedly, we did not observe a better tolerance of city colonies to cadmium, contrary to our previous study, which prevented us from disentangling the respective contributions of workers and larvae to cadmium tolerance. Interestingly, forest colonies seemed to be of better quality in our laboratory conditions. Finally, colony size increased adult survival, but only in the absence of cadmium, suggesting that social buffering could collapse with strong external disturbances.

Extreme lifespan extension in tapeworm-infected ant workers.

Social insects are hosts of diverse parasites, but the influence of these parasites on phenotypic host traits is not yet well understood. Here, we tracked the survival of tapeworm-infected ant workers, their uninfected nest-mates and of ants from unparasitized colonies. Our multi-year study on the ant Temnothorax nylanderi, the intermediate host of the tapeworm Anomotaenia brevis, revealed a prolonged lifespan of infected workers compared with their uninfected peers. Intriguingly, their survival over 3 years did not differ from those of (uninfected) queens, whose lifespan can reach two decades. By contrast, uninfected workers from parasitized colonies suffered from increased mortality compared with uninfected workers from unparasitized colonies. Infected workers exhibited a metabolic rate and lipid content similar to young workers in this species, and they received more social care than uninfected workers and queens in their colonies. This increased attention could be mediated by their deviant chemical profile, which we determined to elicit more interest from uninfected nest-mates in a separate experiment. In conclusion, our study demonstrates an extreme lifespan extension in a social host following tapeworm infection, which appears to enable host workers to retain traits typical for young workers.

Worker Size Diversity Has No Effect on Overwintering Success under Natural Conditions in the Ant Temnothorax nylanderi.

Simple SummaryWinter is a harsh season for organisms living in temperate zones. Winter is often associated with starvation and cold temperatures, and these pressures can strongly affect organism survival. Living in groups can help these animals to cope with winter pressures. Social groups contain individuals which can vary in different ways: physiology, behavior, morphology, etc. In social insects such as ants, worker size leads to different responses to starvation and cold temperature in the laboratory. In this study, we investigated whether worker size affects colony and individual survival under natural conditions. We manipulated both worker size diversity and mean worker size within colonies of the ant Temnothorax nylanderi, reintroduced them in the field, and measured colony survival after overwintering. We found similar colony and individual (both adults and young) survival during winter between treatment colonies with reduced size diversity and/or manipulated mean worker size compared to control colonies with unmanipulated worker size. This result highlights that worker size diversity has no influence on colony performance in this species and more broadly questions the interest of worker size in social insect species with moderate worker size diversity. We discuss the potential sources of worker size diversity, including social context and selfish behavior.Winter is a difficult period for animals that live in temperate zones. It can inflict high mortality or induce weight loss with potential consequences on performance during the growing season. Social groups include individuals of various ages and sizes. This diversity may improve the ability of groups to buffer winter disturbances such as starvation or cold temperature. Studies focusing on the buffering role of social traits such as mean size and diversity of group members under winter conditions are mainly performed in the laboratory and investigate the effect of starvation or cold separately. Here, we experimentally decreased worker size diversity and manipulated worker mean size within colonies in order to study the effect on overwintering survival in the ant Temnothorax nylanderi. Colonies were placed under natural conditions during winter. Colony survival was high during winter and similar in all treatments with no effect of worker size diversity and mean worker size. Higher brood survival was positively correlated with colony size (i.e., the number of workers). Our results show that the higher resistance of larger individuals against cold or starvation stresses observed in the laboratory does not directly translate into higher colony survival in the field. We discuss our results in the light of mechanisms that could explain the possible non-adaptive size diversity in social species.

Social isolation causes downregulation of immune and stress response genes and behavioural changes in a social insect.

Humans and other social mammals experience isolation from their group as stressful, triggering behavioural and physiological anomalies that reduce fitness. While social isolation has been intensely studied in social mammals, it is less clear how social insects, which evolved sociality independently, respond to isolation. Here we examined whether the typical mammalian responses to social isolation, e.g., an impaired ability to interact socially and immune suppression are also found in social insects. We studied the consequences of social isolation on behaviour and brain gene expression in the ant Temnothorax nylanderi. Following isolation, workers interacted moderately less with adult nestmates, increased the duration of brood contact, and reduced the time spent self-grooming, an important sanitary behaviour. Our brain transcriptome analysis revealed that only a few behaviour-related genes had altered their expression with isolation time. Rather, many genes linked to immune system functioning and stress response had been downregulated. This probably sensitizes isolated individuals to various stressors, in particular because isolated workers exhibit reduced sanitary behaviour. We provide evidence of the diverse consequences of social isolation in social insects, some of which resemble those found in social mammals, suggesting a general link between social well-being, stress tolerance, and immune competence in social animals.

Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity.

Most species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant Temnothorax nylanderi, the intermediate host of the cestode Anomotaenia brevis. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes’ transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.

Large body size variation is associated with low communication success in tandem running ants

Diversity in animal groups is often assumed to increase group performance. In insect colonies, genetic, behavioural and morphological variation among workers can improve colony functioning and resilience. However, it has been hypothesized that during communication processes, differences between workers, e.g. in body size, could also have negative effects. Tandem running is a common recruitment strategy in ants and allows a leader to guide a nestmate follower to resources. A substantial proportion of tandem runs fail because leader and follower lose contact. Using the ant Temnothorax nylanderi as a model system, we tested the hypothesis that tandem running success is impaired if leader and follower differ in size. Indeed, we found that the success rate of tandem pairs drops considerably as size variation increases: tandem runs were unsuccessful when the leader–follower size difference exceeded 10%, whereas ~ 80% of tandem runs were successful when ants differed less than 5% in body length. Possible explanations are that size differences are linked to differences in walking speed or sensory perception. Ants did not choose partners of similar size, but extranidal workers were larger than intranidal workers, which could reduce recruitment mistakes because it reduced the chance that very large and very small ants perform tandem runs together. Our results suggest that phenotypic differences between interacting workers can have negative effects on the efficiency of communication processes. Whether phenotypic variation has positive or negative effects is likely to depend on the task and the phenotypic trait that shows variation.Significance statementDiversity is often assumed to increase colony performance in social insects. However, phenotypic differences among workers could also have negative effects, e.g. during communication. Tandem running is a common recruitment strategy in ants, but tandem runs often fail when ants lose contact. We used the ant Temnothorax nylanderi to test the hypothesis that body size differences between tandem leader and follower impair tandem communication. We show that the success rate of tandem pairs drops considerably as size variation increases, possibly because ants of varying size also differ in walking speed. Our study supports the hypothesis that phenotypic variation among workers might not always be beneficial and can negatively impact the efficiency of communication processes.

Manipulation of worker size diversity does not affect colony fitness under natural conditions in the ant Temnothorax nylanderi

In social insects, within-colony worker diversity has long been thought to improve colony fitness. Recent studies start to question this assertion in species with moderate diversity. However, demonstrating an absence of effect is difficult as this absence could be due to the measurement of only few life history traits or to artificial conditions. In order to circumvent these limitations, we experimentally decreased worker size diversity within colonies of the ant Temnothorax nylanderi, with or without affecting mean worker size and we reintroduced them in the field for 4 months (spring and early summer). We then thoroughly measured their fitness based on survival, growth, and reproductive success. Our results show that our manipulation did not affect colony fitness. In addition, colonies did not restore diversity to its initial level, further suggesting that worker size diversity is not a key parameter to them. We found the classically observed positive relationship between colony size, colony growth, and reproductive success. Overall, our results confirm that worker size diversity within colony is not necessarily adaptive in species where it is moderate. We discuss the alternative mechanisms that could explain the evolutionary persistence of moderate worker size diversity. Organisms that live in groups can greatly benefit from the emergence of novel group-level traits. For instance, social insects show significant variability in worker size within colonies. This size diversity increases the division of labor among workers and improves colony fitness. However, in species where size diversity is moderate, this relationship may not always be verified. Here, we manipulated both worker size diversity and mean worker size within colonies of the ant Temnothorax nylanderi, we reintroduced them in the field, and we extensively measured colony fitness after 4 months. We found no impact on colony survival, growth, and reproduction. We discuss how social life and its associated cooperation and conflicts could cause variation in worker size, without any positive effect on colony fitness.

What are the Mechanisms Behind a Parasite-Induced Decline in Nestmate Recognition in Ants?

Social insects have developed sophisticated recognition skills to defend their nests against intruders. They do this by aggressively discriminating against non-nestmates with deviant cuticular hydrocarbon (CHC) signatures. Studying nestmate recognition can be challenging as individual insects do not only vary in their discriminatory abilities, but also in their motivation to behave aggressively. To disentangle the influence of signaling and behavioral motivation on nestmate recognition, we investigated the ant Temnothorax nylanderi, where the presence of tapeworm-infected nestmates leads to reduced nestmate recognition among uninfected workers. The parasite-induced decline in nestmate recognition could be caused by higher intra-colonial cue diversity as tapeworm-infected workers are known to exhibit a modified hydrocarbon signature. This in turn may broaden the neuronal template of their nestmates, leading to a higher tolerance towards alien conspecifics. To test this hypothesis, we exchanged infected ants between colonies and analyzed their impact on CHC profiles of uninfected workers. We demonstrate that despite frequent grooming, which should promote the transfer of recognition cues, CHC profiles of uninfected workers neither changed in the presence of tapeworm-infected ants, nor did it increase cue diversity among uninfected nestmates within or between colonies. However, CHC profiles were systematically affected by the removal of nestmates and addition of non-nestmates, independently from the ants' infection status. For example, when non-nestmates were present workers expressed more dimethyl alkanes and higher overall CHC quantities, possibly to achieve a better distinction from non-nestmates. Workers showed clear task-specific profiles with tapeworm-infected workers resembling more closely young nurses than older foragers. Our results show that the parasite-induced decline in nestmate recognition is not due to increased recognition cue diversity or altered CHC profiles of uninfected workers, but behavioral changes might explain tolerance towards intruders.

Decreasing worker size diversity does not affect colony performance during laboratory challenges in the ant Temnothorax nylanderi

Within-colony phenotypic diversity can play an essential role in some eusocial insect taxa by increasing the performance of division of labor, thereby increasing colony fitness. Empirical studies of the effect of phenotypic diversity on colony fitness mostly focused on species with discrete castes (workers, soldiers) or with continuously and highly morphologically variable workers, which is not the most common case. Indeed, most species exhibit continuous but limited worker morphological variation. It is still unclear whether this variation impacts colony fitness. To test this, we reduced the worker size diversity in 25 colonies of the ant Temnothorax nylanderi and compared their performances to 25 control colonies. We reared these colonies in the laboratory and measured the effect of treatment (reduced diversity or control) and colony size (number of workers) on colony performance at six challenges, as well as on worker mortality and brood production. The reduction of worker size diversity did not affect colony performance nor mortality and brood production. As expected, colony performance and brood production increased with colony size. These results suggest that worker size diversity may not be under positive selection in this species, but rather the product of a lack of developmental canalization. We propose that social life could decrease the selective pressures maintaining developmental canalization, subsequently leading to higher size diversity without necessarily increasing colony performance.

Effect of temperature and social environment on worker size in the ant Temnothorax nylanderi

Warm temperatures decrease insect developmental time and body size. Social life could buffer external environmental variations, especially in large social groups, either through behavioral regulation and compensation or through specific nest architecture. Mean worker size and distribution of worker sizes within colonies are important parameters affecting colony productivity as worker size is linked to division of labor in insect societies. In this paper, we investigate the effect of stressful warm temperatures and the role of social environment (colony size and size of nestmate workers) on the mean size and size variation of laboratory-born workers in the small European ant Temnothorax nylanderi. To do so, we reared field-collected colonies under medium or warm temperature treatments after having marked the field-born workers and removed the brood except for 30 first instar larvae. Warm temperature resulted in the production of fewer workers and a higher adult mortality, confirming that this regime was stressful for the ants. T. nylanderi ants followed the temperature size rule observed in insects, with a decreased developmental time and mean size under warm condition. Social environment appeared to play an important role as we observed that (i) larger colonies buffered the effect of temperature better than smaller ones (ii) colonies with larger workers produced larger workers whatever the rearing temperature and (iii) the coefficient of variation of worker size was similar in the field and under medium laboratory temperature. This suggests that worker size variation is not primarily due to seasonal environmental fluctuations in the field. Finally, we observed a higher coefficient of variation of worker size under warm temperature. We propose that this results from a disruption of social regulation, i.e. the control of nestmate workers over developing larvae and adult worker size, under stressful conditions.

Starvation endurance in the ant Temnothorax nylanderi depends on group size, body size and access to larvae

Social interactions in animal groups can buffer environmental stress and may enhance survival under unfavourable conditions. In the present study, the impact on starvation endurance of social group, access to larvae and cold shock is studied in the ant Temnothorax nylanderi Förster. Resource sharing is expected to lead to grouped workers surviving longer than isolated ones. Access to larvae may increase longevity if larvae serve as food, or may interfere with survival if they induce caring behaviour in workers. Cold shock serves as a stress factor and a negative influence on survival is expected. The results show that isolated workers have a shorter lifespan than grouped workers, which in turn live for a shorter period than grouped workers with larvae. Beneficial ‘group effects’ contribute to group survival and the presence of larvae increases worker survival because the workers presumably feed on the larvae. Thus, improved starvation endurance may reflect an additional benefit of a social lifestyle. Moreover, variance in survival is lower for grouped workers than for isolated workers: group members not only demonstrate improved survival, but also smaller within‐group differences. Although a negative influence on survival is the expected outcome, this type of thermal stress is found to have no direct impact on starvation endurance other than moderating the differences between isolated and grouped workers.

Hierarchy length in orphaned colonies of the ant Temnothorax nylanderi

Workers of the ant Temnothorax nylanderi form dominance orders in orphaned colonies in which only one or a few top-ranking workers begin to produce males from unfertilized eggs. Between one and 11 individuals initiated 80% of all aggression in 14 queenless colonies. As predicted from inclusive fitness models (Molet M, van Baalen M, Monnin T, Insectes Soc 52:247-256, 2005), hierarchy length was found to first increase with colony size and then to level off at larger worker numbers. The frequency and skew of aggression decreased with increasing size, indicating that rank orders are less pronounced in larger colonies.