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.

The effects of disturbance threat on leaf-cutting ant colonies: a laboratory study.

The flexibility of organisms to respond plastically to their environment is fundamental to their fitness and evolutionary success. Social insects provide some of the most impressive examples of plasticity, with individuals exhibiting behavioral and sometimes morphological adaptations for their specific roles in the colony, such as large soldiers for nest defense. However, with the exception of the honey bee model organism, there has been little investigation of the nature and effects of environmental stimuli thought to instigate alternative phenotypes in social insects. Here, we investigate the effect of repeated threat disturbance over a prolonged (17 month) period on both behavioral and morphological phenotypes, using phenotypically plastic leaf-cutting ants (Atta colombica) as a model system. We found a rapid impact of threat disturbance on the behavioral phenotype of individuals within threat-disturbed colonies becoming more aggressive, threat responsive, and phototactic within as little as 2 weeks. We found no effect of threat disturbance on morphological phenotypes, potentially, because constraints such as resource limitation outweighed the benefit for colonies of producing larger individuals. The results suggest that plasticity in behavioral phenotypes can enable insect societies to respond to threats even when constraints prevent alteration of morphological phenotypes.

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.

Behavioural development, fat reserves and their association with productivity in Lasius flavus founding queens.

Reproduction-related behaviours are key components determining individual fitness. Many behavioural traits are linked, and such trait associations often affect fitness. Here, we combine behavioural and physiological data during two critical time points of founding queens (early and late nest-founding stage) in the claustral ant Lasius flavus to assess how these factors affect their initial productivity. We show that most behavioural traits, except brood care behaviour, are plastic during queen development and demonstrate that there are alternative behavioural pathways to achieve high productivity under standardised conditions. These results indicate that queens can utilise multiple behavioural trait combinations to maximise reproductive output at the earliest, and arguably most critical, time of colony foundation.

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.

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.

Isoform-specific increase of spastin stability by N-terminal missense variants including intragenic modifiers of SPG4 hereditary spastic paraplegia.

Hereditary spastic paraplegia (HSP) is a neurodegenerative disorder selectively affecting axons of spinal cord motoneurons. Classical mutations in the most frequent HSP gene SPAST (spastin protein) act through haploinsufficiency by abolishing the activity of a C-terminal ATPase domain or by interfering with expression from the affected allele. N-terminal missense variants have been suggested to represent rare polymorphisms, to cause unusually mild phenotypes, and to aggravate the effect of a classical mutation. We confirm these associations for p.S44L but do not detect two other variants (p.E43Q; p.P45Q) in HSP patients and controls. We show that neither of several disease mechanisms associated with classical SPAST mutations applies to the N-terminal variants. Instead, all three alterations enhance the stability of one of two alternative spastin isoforms. Their phenotypic effect may thus not be mediated by haploinsufficiency but by increasing isoform competition for interacting proteins, substrates or oligomerization partners.

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.