Sex-Specific Effect of the Dietary Protein to Carbohydrate Ratio on Personality in the Dubia Cockroach.

Animal personality, defined by behavioral variations among individuals consistent over contexts or time, is shaped by genetic and environmental factors. Among these factors, nutrition can play an important role. The Geometric Framework of Nutrition has promoted a better understanding of the role of the macronutrient proportion in animal development, survival, reproduction, and behavior, and can help to disentangle its modulatory effect on animal personality. In this study, we investigated the effects of protein to carbohydrate (P:C) ratio in the personality of the cockroach Blaptica dubia. Newly emerged adults were fed over a period of eight weeks on five different diets varying in their P:C ratio and their diet consumption, mass variation, survival, exploratory behavior, and mobility were assessed. We found that females, unlike males, were able to regulate their nutrient intake and preferred carbohydrate-rich diets. Females also gained more body mass and lived longer compared to males. In addition, their behavior and mobility were not affected by the diet. In males, however, high-protein diets induced a bolder personality. We suggest that the sex-specific effects observed on both survival and behavior are related to the nutrient intake regulation capacity and might improve the species' fitness in adverse nutritional conditions.

Insect lifestyle and evolution of brain morphology.

Insect lifestyles are extremely diversified and have important consequences for brain function. Lifestyle determines the resources and information that brains might access and also those that are required to produce adaptive behaviors. Most of the observed adaptations in brain morphology to variation in lifestyle are related to the first stages of sensory information processing (e.g. adaptations to diel habits). However, morphological signatures of lifestyles related to higher order processing of information are more difficult to demonstrate. Co-option of existing neural structures for new behaviors might hinder the detection of morphological changes at a large scale. Current methodological advances will make it possible to investigate finer structural changes (e.g. variation in the connectivity between neurons) and might shed light on whether or not some lifestyles (e.g. eusociality) require morphological adaptations.

The neuroplasticity of division of labor: worker polymorphism, compound eye structure and brain organization in the leafcutter ant Atta cephalotes.

Our understanding of how sensory structure design is coupled with neural processing capacity to adaptively support division of labor is limited. Workers of the remarkably polymorphic fungus-growing ant Atta cephalotes are behaviorally specialized by size: the smallest workers (minims) tend fungi in dark subterranean chambers while larger workers perform tasks outside the nest. Strong differences in worksite light conditions are predicted to influence sensory and processing requirements for vision. Analyzing confocal scans of worker eyes and brains, we found that eye structure and visual neuropils appear to have been selected to maximize task performance according to light availability. Minim eyes had few ommatidia, large interommatidial angles and eye parameter values, suggesting selection for visual sensitivity over acuity. Large workers had larger eyes with disproportionally more and larger ommatidia, and smaller interommatidial angles and eye parameter values, indicating peripheral sensory adaptation to ambient rainforest light. Optic lobes and mushroom body collars were disproportionately small in minims. Within the optic lobe, lamina and lobula relative volumes increased with worker size whereas medulla volume decreased. Visual system phenotypes thus correspond to task specializations in dark or light environments and illustrate a functional neuroplasticity underpinning division of labor in this socially complex agricultural ant.

Correction: Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians.

[This corrects the article DOI: 10.1371/journal.pone.0213618.].

Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians.

Strongly polyphenic social insects provide excellent models to examine the neurobiological basis of division of labor. Turtle ants, Cephalotes varians, have distinct minor worker, soldier, and reproductive (gyne/queen) morphologies associated with their behavioral profiles: small-bodied task-generalist minors lack the phragmotic shield-shaped heads of soldiers, which are specialized to block and guard the nest entrance. Gynes found new colonies and during early stages of colony growth overlap behaviorally with soldiers. Here we describe patterns of brain structure and synaptic organization associated with division of labor in C. varians minor workers, soldiers, and gynes. We quantified brain volumes, determined scaling relationships among brain regions, and quantified the density and size of microglomeruli, synaptic complexes in the mushroom body calyxes important to higher-order processing abilities that may underpin behavioral performance. We found that brain volume was significantly larger in gynes; minor workers and soldiers had similar brain sizes. Consistent with their larger behavioral repertoire, minors had disproportionately larger mushroom bodies than soldiers and gynes. Soldiers and gynes had larger optic lobes, which may be important for flight and navigation in gynes, but serve different functions in soldiers. Microglomeruli were larger and less dense in minor workers; soldiers and gynes did not differ. Correspondence in brain structure despite differences in soldiers and gyne behavior may reflect developmental integration, suggesting that neurobiological metrics not only advance our understanding of brain evolution in social insects, but may also help resolve questions of the origin of novel castes.

Origins of Aminergic Regulation of Behavior in Complex Insect Social Systems.

Neuromodulators are conserved across insect taxa, but how biogenic amines and their receptors in ancestral solitary forms have been co-opted to control behaviors in derived socially complex species is largely unknown. Here we explore patterns associated with the functions of octopamine (OA), serotonin (5-HT) and dopamine (DA) in solitary ancestral insects and their derived functions in eusocial ants, bees, wasps and termites. Synthesizing current findings that reveal potential ancestral roles of monoamines in insects, we identify physiological processes and conserved behaviors under aminergic control, consider how biogenic amines may have evolved to modulate complex social behavior, and present focal research areas that warrant further study.

Parsing the life-shortening effects of dietary protein: effects of individual amino acids.

High-protein diets shorten lifespan in many organisms. Is it because protein digestion is energetically costly or because the final products (the amino acids) are harmful? To answer this question while circumventing the life-history trade-off between reproduction and longevity, we fed sterile ant workers on diets based on whole proteins or free amino acids. We found that (i) free amino acids shortened lifespan even more than proteins; (ii) the higher the amino acid-to-carbohydrate ratio, the shorter ants lived and the lower their lipid reserves; (iii) for the same amino acid-to-carbohydrate ratio, ants eating free amino acids had more lipid reserves than those eating whole proteins; and (iv) on whole protein diets, ants seem to regulate food intake by prioritizing sugar, while on free amino acid diets, they seem to prioritize amino acids. To test the effect of the amino acid profile, we tested diets containing proportions of each amino acid that matched the ant's exome; surprisingly, longevity was unaffected by this change. We further tested diets with all amino acids under-represented except one, finding that methionine, serine, threonine and phenylalanine are especially harmful. All together, our results show certain amino acids are key elements behind the high-protein diet reduction in lifespan.

idTracker: tracking individuals in a group by automatic identification of unmarked animals.

Animals in groups touch each other, move in paths that cross, and interact in complex ways. Current video tracking methods sometimes switch identities of unmarked individuals during these interactions. These errors propagate and result in random assignments after a few minutes unless manually corrected. We present idTracker, a multitracking algorithm that extracts a characteristic fingerprint from each animal in a video recording of a group. It then uses these fingerprints to identify every individual throughout the video. Tracking by identification prevents propagation of errors, and the correct identities can be maintained indefinitely. idTracker distinguishes animals even when humans cannot, such as for size-matched siblings, and reidentifies animals after they temporarily disappear from view or across different videos. It is robust, easy to use and general. We tested it on fish (Danio rerio and Oryzias latipes), flies (Drosophila melanogaster), ants (Messor structor) and mice (Mus musculus).

A common rule for decision making in animal collectives across species.

A diversity of decision-making systems has been observed in animal collectives. In some species, choices depend on the differences of the numbers of animals that have chosen each of the available options, whereas in other species on the relative differences (a behavior known as Weber's law), or follow more complex rules. We here show that this diversity of decision systems corresponds to a single rule of decision making in collectives. We first obtained a decision rule based on Bayesian estimation that uses the information provided by the behaviors of the other individuals to improve the estimation of the structure of the world. We then tested this rule in decision experiments using zebrafish (Danio rerio), and in existing rich datasets of argentine ants (Linepithema humile) and sticklebacks (Gasterosteus aculeatus), showing that a unified model across species can quantitatively explain the diversity of decision systems. Further, these results show that the different counting systems used by animals, including humans, can emerge from the common principle of using social information to make good decisions.

Sodium pumps adapt spike bursting to stimulus statistics.

Pump activity is a homeostatic mechanism that maintains ionic gradients. Here we examined whether the slow reduction in excitability induced by sodium-pump activity that has been seen in many neuronal types is also involved in neuronal coding. We took intracellular recordings from a spike-bursting sensory neuron in the leech Hirudo medicinalis in response to naturalistic tactile stimuli with different statistical distributions. We show that regulation of excitability by sodium pumps is necessary for the neuron to make different responses depending on the statistical context of the stimuli. In particular, sodium-pump activity allowed spike-burst sizes and rates to code not for stimulus values per se, but for their ratio with the standard deviation of the stimulus distribution. Modeling further showed that sodium pumps can be a general mechanism of adaptation to statistics on the time scale of 1 min. These results implicate the ubiquitous pump activity in the adaptation of neural codes to statistics.