Synergistic effects of pathogen and pesticide exposure on honey bee (Apis mellifera) survival and immunity.

Declines in native insect pollinator populations and substantial losses in managed honey bees have been reported on a global scale and become a widespread concern because of the importance of these insects for human food production and ecosystem stability. Several potential factors have been studied as possible causes of declining pollinator health, such as parasites and pathogens, exposure to agricultural pesticides, habitat loss and/or climate change. More recently, a combination of these factors rather than a single cause have been blamed for observed pollinator losses, but field studies of such interactions are challenging, especially in the presence of confounding environmental stressors. We therefore examined the impact of single and combined stressors on the honey bee (Apis mellifera) in a generally healthy Australian population. We exposed workers during their larval development and drones until they reached sexual maturity to the neonicotinoid pesticide Thiamethoxam, at concentrations more than 20 times lower than we initially measured in the field, the microsporidian gut pathogen Nosema apis or both stressors at the same time. We found that simultaneous exposure significantly reduced bee health. We observed a substantial increase in mortality and a reduction of immunocompetence in workers exposed to both the pathogen and the pesticide. We conclude that the exposure of generally healthy bees to multiple environmental stressors results in synergistic effects where the effects are expected to negatively impact performance and could be sufficient to trigger colony collapse. We found that the vast majority of males did not survive to sexual maturity after exposure to very low levels of Thiamethoxam. This would not only reduce the reproductive success of individual colonies, but can also impact gene flow and genetic diversity at the population level, which are both known as key components of honey bee health.

Physiology of reproductive worker honey bees (Apis mellifera): insights for the development of the worker caste.

Reproductive and behavioural specialisations characterise advanced social insect societies. Typically, the honey bee (Apis mellifera) shows a pronounced reproductive division of labour between worker and queen castes, and a clear division of colony roles among workers. In a queenless condition, however, both of these aspects of social organisation break down. Queenless workers reproduce, forage and maintain their colony operating in a manner similar to communal bees, rather than as an advanced eusocial group. This plasticity in social organisation provides a natural experiment for exploring physiological mechanisms of division of labour. We measured brain biogenic amine (BA) levels and abdominal fat body vitellogenin gene expression levels of workers in queenright and queenless colonies. Age, ovary activation and social environment influenced brain BA levels in honey bees. BA levels were most influenced by ovary activation state in queenless bees. Vitellogenin expression levels were higher in queenless workers than queenright workers, but in both colony environments vitellogenin expression was lower in foragers than non-foragers. We propose this plasticity in the interacting signalling systems that influence both reproductive and behavioural development allows queenless workers to deviate significantly from the typical worker bee reaction norm and develop as reproductively active behavioural generalists.

Experimentally testing mate preference in an avian system with unidirectional bill color introgression.

Mating behavior can play a key role in speciation by inhibiting or facilitating gene flow between closely related taxa. Hybrid zones facilitate a direct examination of mating behavior and the traits involved in establishing species barriers. The long-tailed finch (Poephila acuticauda) has two hybridizing subspecies that differ in bill color (red and yellow), and the yellow bill phenotype appears to have introgressed ~350 km eastward following secondary contact. To examine the role of mate choice on bill color introgression, we performed behavioral assays using natural and manipulated bill colors. We found an assortative female mating preference for males of their own subspecies when bill color was not manipulated. However, we did not find this assortative preference in trials based on artificially manipulated bill color. This could suggest that assortative preference is not fixed entirely on bill color and instead may be based on a different trait (e.g., song) or a combination of traits, or alternatively may be due to lower statistical power alongside the bill manipulations being unconvincing to the female choosers. Intriguingly, we find a bias in the inheritance of bill color in captive bred F1 hybrid females. Previous modeling suggests that assortative mate preference and this kind of partial dominance in the underlying genes may together contribute to introgression, making the genetic architecture of bill color in this system a priority for future research.

Ladies First: Coerced Mating in a Fiddler Crab.

In some species males increase their reproductive success by forcing females to copulate with them, usually by grasping the female or pinning her to the ground to prevent her from escaping. Here we report an example of males coercing copulation by trapping a female in a confined space. During mate-searching, female Uca mjoebergi fiddler crabs visit males and choose whether or not to enter their burrow for inspection. Males typically enter the burrow first and we found that 71% of females will follow him down and 54% decide to stay and mate. However, some males use an alternative tactic where he will wait for the female to enter the burrow first, after which he traps her inside. Although a significantly lower percentage of females will enter a burrow following this behaviour (41%), upon entry 79% females that enter will become trapped and almost all of these females (90%) produce a clutch of eggs. Our observations suggest that males are able to gain fertilisations from females that may not have remained in the burrow by trapping them and coercing them to mate.

Pheromonal control: reconciling physiological mechanism with signalling theory.

Pheromones are intraspecific chemical signals. They can have profound effects on the behaviour and/or physiology of the receiver, and it is still common to hear pheromones described as controlling of the behaviour of the receiver. The discussion of pheromonal control arose initially from a close association between hormones and pheromones in the comparative physiological literature, but the concept of a controlling pheromone is at odds with contemporary signal evolution theory, which predicts that a manipulative pheromonal signal negatively affecting the receiver's fitness should not be stable over evolutionary time. Here we discuss the meaning of pheromonal control, and the ecological circumstances by which it might be supported. We argue that in discussing pheromonal control it is important to differentiate between control applied to the effects of a pheromone on a receiver's physiology (proximate control), and control applied to the effects of a pheromone on a receiver's fitness (ultimate control). Critically, a pheromone signal affecting change in the receiver's behaviour or physiology need not necessarily manipulate the fitness of a receiver. In cases where pheromonal signalling does lead to a reduction in the fitness of the receiver, the signalling system would be stable if the pheromone were an honest signal of a social environment that disadvantages the receiver, and the physiological and behavioural changes observed in the receiver were an adaptive response to the new social circumstances communicated by the pheromone.

Altruistic behavior by egg-laying worker honeybees.

If a honeybee (Apis mellifera) colony loses its queen, worker bees develop their ovaries and produce male offspring [1]. Kin selection theory predicts that the degree of altruism in queenless colonies should be reduced because the relatedness of workers to a hivemate's offspring is less in queenless colonies than it is to the daughters of the queen in queenright colonies [2-4]. To explore this hypothesis, we examined the behavior and physiology of queenless egg-laying workers. Queenless bees engaged in both personal reproduction and the social foraging and defense tasks that benefited their colony. Laying workers also had larger brood-food-producing and wax glands, showing metabolic investments in both colony maintenance and personal reproduction. Whereas in queenright colonies there is a very clear age-based pattern of division of labor between workers, in queenless colonies the degree of individual specialization was much reduced. Queenless colonies functioned as a collective of reproductive and behaviorally generalist bees that cooperatively maintained and defended their nest. This social structure is similar to that observed in a number of primitively social bee species [5]. Laying workers therefore show a mix of selfish personal reproduction and altruistic cooperative behavior, and the queenless state reveals previously unrecognized plasticity in honeybee social organization.