Tobias Pamminger

Pleiotropic effects of juvenile hormone in ant queens and the escape from the reproduction–immunocompetence trade-off

The ubiquitous trade-off between survival and costly reproduction is one of the most fundamental constraints governing life-history evolution. In numerous animals, gonadotropic hormones antagonistically suppressing immunocompetence cause this trade-off. The queens of many social insects defy the reproduction–survival trade-off, achieving both an extraordinarily long life and high reproductive output, but how they achieve this is unknown. Here we show experimentally, by integrating quantification of gene expression, physiology and behaviour, that the long-lived queens of the ant Lasius niger have escaped the reproduction–immunocompetence trade-off by decoupling the effects of a key endocrine regulator of fertility and immunocompetence in solitary insects, juvenile hormone (JH). This modification of the regulatory architecture enables queens to sustain a high reproductive output without elevated JH titres and suppressed immunocompetence, providing an escape from the reproduction–immunocompetence trade-off that may contribute to the extraordinary lifespan of many social insect queens.

Oh sister, where art thou? Spatial population structure and the evolution of an altruistic defence trait

The evolution of parasite virulence and host defences is affected by population structure. This effect has been confirmed in studies focusing on large spatial scales, whereas the importance of local structure is not well understood. Slavemaking ants are social parasites that exploit workers of another species to rear their offspring. Enslaved workers of the host species Temnothorax longispinosus have been found to exhibit an effective post‐enslavement defence behaviour: enslaved workers were observed killing a large proportion of the parasites’ offspring. As enslaved workers do not reproduce, they gain no direct fitness benefit from this ‘rebellion’ behaviour. However, there may be an indirect benefit: neighbouring host nests that are related to ‘rebel’ nests can benefit from a reduced raiding pressure, as a result of the reduction in parasite nest size due to the enslaved workers’ killing behaviour. We use a simple mathematical model to examine whether the small‐scale population structure of the host species could explain the evolution of this potentially altruistic defence trait against slavemaking ants. We find that this is the case if enslaved host workers are related to nearby host nests. In a population genetic study, we confirm that enslaved workers are, indeed, more closely related to host nests within the raiding range of their resident slavemaker nest, than to host nests outside the raiding range. This small‐scale population structure seems to be a result of polydomy (e.g. the occupation of several nests in close proximity by a single colony) and could have enabled the evolution of ‘rebellion’ by kin selection.

Hygienic food to reduce pathogen risk to bumblebees

Bumblebees are ecologically and economically important pollinators, and the value of bumblebees for crop pollination has led to the commercial production and exportation/importation of colonies on a global scale. Commercially produced bumblebee colonies can carry with them infectious parasites, which can both reduce the health of the colonies and spillover to wild bees, with potentially serious consequences. The presence of parasites in commercially produced bumblebee colonies is in part because colonies are reared on pollen collected from honey bees, which often contains a diversity of microbial parasites. In response to this threat, part of the industry has started to irradiate pollen used for bumblebee rearing. However, to date there is limited data published on the efficacy of this treatment. Here we examine the effect of gamma irradiation and an experimental ozone treatment on the presence and viability of parasites in honey bee pollen. While untreated pollen contained numerous viable parasites, we find that gamma irradiation reduced the viability of parasites in pollen, but did not eliminate parasites entirely. Ozone treatment appeared to be less effective than gamma irradiation, while an artificial pollen substitute was, as expected, entirely free of parasites. The results suggest that the irradiation of pollen before using it to rear bumblebee colonies is a sensible method which will help reduce the incidence of parasite infections in commercially produced bumblebee colonies, but that further optimisation, or the use of a nutritionally equivalent artificial pollen substitute, may be needed to fully eliminate this route of disease entry into factories.

The effects of juvenile hormone on Lasius niger reproduction.

Reproduction has been shown to be costly for survival in a wide diversity of taxa. The resulting trade-off, termed the reproduction-survival trade-off, is thought to be one of the most fundamental forces of life-history evolution. In insects the pleiotropic effect of juvenile hormone (JH), antagonistically regulating reproduction and pathogen resistance, is suggested to underlie this phenomenon. In contrast to the majority of insects, reproductive individuals in many eusocial insects defy this trade-off and live both long and prosper. By remodelling the gonadotropic effects of JH in reproductive regulation, the queens of the long-lived black garden ant Lasius niger (living up to 27 years), have circumvented the reproduction-survival trade off enabling them to maximize both reproduction and pathogen resistance simultaneously. In this study we measure fertility, vitellogenin gene expression and protein levels after experimental manipulation of hormone levels. We use these measurements to investigate the mechanistic basis of endocrinological role remodelling in reproduction and determine how JH suppresses reproduction in this species, rather then stimulating it, like in the majority of insects. We find that JH likely inhibits three key aspects of reproduction both during vitellogenesis and oogenesis, including two previously unknown mechanisms. In addition, we document that juvenile hormone, as in the majority of insects, has retained some stimulatory function in regulating vitellogenin expression. We discuss the evolutionary consequences of this complex regulatory architecture of reproduction in L. niger, which might enable the evolution of similar reproductive phenotypes by alternate regulatory pathways, and the surprising flexibility regulatory role of juvenile hormone in this process.

High temperature and temperature variation undermine future disease susceptibility in a population of the invasive garden ant Lasius neglectus.

Environmental temperature and temperature variation can have strong effects on the outcome of host-parasite interactions. Whilst such effects have been reported for different host systems, long-term consequences of pre-infection temperatures on host susceptibility and immunity remain understudied. Here, we show that experiencing both a biologically relevant increase in temperature and temperature variation undermines future disease susceptibility of the invasive garden ant Lasius neglectus when challenged with a pathogen under a constant temperature regime. In light of the economic and ecological importance of many social insects, our results emphasise the necessity to take the hosts’ temperature history into account when studying host-parasite interactions under both natural and laboratory conditions, especially in the face of global change.

Testing the reproductive groundplan hypothesis in ants (Hymenoptera: Formicidae)

The evolution of complex societies with obligate reproductive division of labor represents one of the major transitions in evolution. In such societies, functionally sterile individuals (workers) perform many of fitness‐relevant behaviors including allomaternal ones, without getting any direct fitness benefits. The question of how such worker division of labor has evolved remains controversial. The reproductive groundplan hypothesis (RGPH) offers a powerful proximate explanation for this evolutionary leap. The RGPH argues that the conserved genetic and endocrinological networks regulating fitness‐relevant behavior (e g. foraging and brood care) in their solitary ancestors have become decoupled from actual reproduction in the worker caste and now generate worker behavioral phenotypes. However, the empirical support for this hypothesis remains limited to a handful of species making its general validity uncertain. In this study, we combine data from the literature with targeted sampling of key species and apply phylogenetically controlled comparative analysis to investigate if the key prediction of the RGPH, namely an association between allomaternal behavior and an allomaternal physiological state holds in the largest and most species‐rich clade of social insects, the ants. Our findings clearly support the RPGH as a general framework to understand the evolution of the worker caste and shed light on one of the major transition in evolutionary history.

The evolution of caste-biasing symbionts in the social hymenoptera

The separation of individuals into reproductive and worker castes is the defining feature of insect societies. However, caste determination is itself a complex phenomenon, dependent on interacting genetic and environmental factors. It has been suggested by some authors that widespread maternally transmitted symbionts such as Wolbachia may be selected to interfere with caste determination, whilst others have discounted this possibility on theoretical grounds. We argue that there are in fact three distinct evolutionary scenarios in which maternally transmitted symbionts might be selected to influence the process of caste determination in a social hymenopteran host. Each of these scenarios generate testable predictions which we outline here. Given the increasing recognition of the complexity and multi-faceted nature of caste determination in social insects, we argue that maternally transmitted symbionts should also be considered as possible factors influencing the development of social hymenopterans.

A mechanistic framework to explain the immunosuppressive effects of neurotoxic pesticides on bees

1. There is growing concern that declines in some managed and wild bee pollinator populations threaten biodiversity, the functioning of vital ecological processes and sustainable food production on a global scale. 2. In recent years, there has been increasing evidence that sub-lethal exposure to the neurotoxic class of insecticides (neonicotinoids) can undermine pollinator immunocompetence and amplify the effects of diseases, which have been suspected to be one of the drivers of pollinator declines. However, exactly how neonicotinoids might inhibit pollinator immunity remains elusive. 3. Here we put forward a mechanistic framework to explain the effects of neurotoxic pesticides on insect immunocompetence. We propose that there is a close ontogenetic connection between the cellular arm (haemocytes) of the insect immune and nervous systems, and that this connection makes the immune system of pollinators and other insects inherently susceptible to interference by neurotoxins such as neonicotinoids at sublethal doses. 4. Investigation of this connection is urgently needed to confirm the validity of this framework, and develop a clear, mechanistically-informed understanding of the interplay between neonicotinoids and disease ecology in pollinators. This in turn may enable us to develop strategies to mitigate impacts of neurotoxins on pollinators and/or enhance their impacts on pests.

Social environment affects the transcriptomic response to bacteria in ant queens

Abstract Social insects have evolved enormous capacities to collectively build nests and defend their colonies against both predators and pathogens. The latter is achieved by a combination of individual immune responses and sophisticated collective behavioral and organizational disease defenses, that is, social immunity. We investigated how the presence or absence of these social defense lines affects individual‐level immunity in ant queens after bacterial infection. To this end, we injected queens of the ant Linepithema humile with a mix of gram+ and gram− bacteria or a control solution, reared them either with workers or alone and analyzed their gene expression patterns at 2, 4, 8, and 12 hr post‐injection, using RNA‐seq. This allowed us to test for the effect of bacterial infection, social context, as well as the interaction between the two over the course of infection and raising of an immune response. We found that social isolation per se affected queen gene expression for metabolism genes, but not for immune genes. When infected, queens reared with and without workers up‐regulated similar numbers of innate immune genes revealing activation of Toll and Imd signaling pathways and melanization. Interestingly, however, they mostly regulated different genes along the pathways and showed a different pattern of overall gene up‐regulation or down‐regulation. Hence, we can conclude that the absence of workers does not compromise the onset of an individual immune response by the queens, but that the social environment impacts the route of the individual innate immune responses.

First indication of acetylcholine-based communication in honeybee haemocytes and its modulation by a neonicotinoid insecticide

There is growing concern that some managed and wild insect pollinator populations are in decline, potentially threatening biodiversity and sustainable food production on a global scale. In recent years, there has been increasing evidence that sub-lethal exposure to neurotoxic, neonicotinoid pesticides can negatively affect pollinator immunocompetence and amplify the effects of diseases, likely contributing to pollinator declines. Here we show that a range of non-neural tissues and haemocytes of the honeybee Apis mellifera express the nicotinic acetylcholine receptor that is the target of neonicotinoids. In addition, we demonstrate that the haemocytes, which form the cellular arm of the innate immune system, actively synthesize acetylcholine. This suggests the presence of a neural-independent acetylcholine-based immune signalling system in insects similar to that found in vertebrates. Lastly we establish that field-relevant doses of the neonicotinoid insecticide clothianidin alter this communication system. These findings provide a novel, mechanistically informed framework to understand the numerous siede-effects on insects of sub-lethal pesticide exposure, including immunosuppression. They support the growing evidence for acetylcholine-based immune regulation in invertebrates that operates independently of the nervous system.