Pollen reinforces learning in honey bee pollen foragers but not in nectar foragers

ABSTRACTSearching for reward motivates and drives behaviour. In honey bees Apis mellifera, specialized pollen foragers are attracted to and learn odours with pollen. However, the role of pollen as a reward remains poorly understood. Unlike nectar, pollen is not ingested during collection. We hypothesized that pollen (but not nectar) foragers could learn pollen by sole antennal or tarsal stimulation. Then, we tested how pairing of pollen (either hand- or bee-collected) and a neutral odour during a pre-conditioning affects performance of both pollen and nectar foragers during the classical conditioning of the proboscis extension response. Secondly, we tested whether nectar and pollen foragers perceive the simultaneous presentation of pollen (on the tarsi) and sugar (on the antennae) as a better reinforcement than sucrose alone. Finally, we searched for differences in learning of the pollen and nectar foragers when they were prevented from ingesting the reward during the conditioning. Differences in pollen-reinforced learning correlate with division of labour between pollen and nectar foragers. Results show that pollen foragers performed better than nectar foragers during the conditioning phase after being pre-conditioned with pollen. Pollen foragers also performed better than nectar foragers in both the acquisition and extinction phases of the conditioning, when reinforced with the dual reward. Consistently, pollen foragers showed improved abilities to learn cues reinforced without sugar ingestion. We discussed that differences in how pollen and nectar foragers respond to a cue associated with pollen greatly contribute to the physiological mechanism that underlies foraging specialization in the honeybee.

Competitive advantage of rare behaviours induces adaptive diversity rather than social conformity in skill learning

Recent studies have emphasized the role of social learning and cultural transmission in promoting conformity and uniformity in animal groups, but little attention has been given to the role of negative frequency-dependent learning in impeding conformity and promoting diversity instead. Here, we show experimentally that under competitive conditions that are common in nature, social foragers (although capable of social learning) are likely to develop diversity in foraging specialization rather than uniformity. Naive house sparrows that were introduced into groups of foraging specialists did not conform to the behaviour of the specialists, but rather learned to use the alternative food-related cues, thus forming groups of complementary specialists. We further show that individuals in such groups may forage more effectively in diverse environments. Our results suggest that when the benefit from socially acquired skills diminishes through competition in a negative frequency-dependent manner, animal societies will become behaviourally diverse rather than uniform.

In polytocous mammals, weakling neonates, but not their stronger littermates, benefit from specialized foraging

Adjusting foraging strategies is a common phenomenon within groups of animals competing for the same resource. In polytocous mammals, neonates concurrently compete for limited milk and alternate between two foraging (suckling) strategies: adaptable exploratory foraging with random sampling of teats, and ordered foraging with a tendency towards exploiting a particular suckling position. Some theoretical (game theory) models have shown that weaker siblings in particular benefit from foraging specialization (suckling order). Neonate piglets establish a well-defined suckling order that develops gradually and fluctuates throughout the lactation period, implying the existence of inter-individual differences in foraging strategies. We therefore analyzed suckling behavior in pigs to determine whether one foraging strategy was more beneficial to neonates in terms of their body weight and foraging environment. We found that intermediate and heavy littermates tended to adjust their suckling strategy according to the foraging environment; however, the selected foraging strategy did not affect their overall growth performance. Lighter individuals that consumed significantly less milk did not greatly alternate their foraging strategy according to the foraging environment, but their growth rate was significantly higher whenever they performed less-exploratory foraging behavior. Although suckling order appeared to be a relatively stable behavioral phenotype, it was beneficial exclusively for weaklings. These results confirm theoretical predictions and indicate that specializing in a suckling position is a beneficial strategy for weaker, light neonates. These findings suggest that physically weaker neonates might have driven the evolution of neonatal foraging specialization.

Genetic and developmental origins of a unique foraging adaptation in a Lake Malawi cichlid genus

Phenotypic novelties are an important but poorly understood category of morphological diversity. They can provide insights into the origins of phenotypic variation, but we know relatively little about their genetic origins. Cichlid fishes display remarkable diversity in craniofacial anatomy, including several novelties. One aspect of this variation is a conspicuous, exaggerated snout that has evolved in a single Malawi cichlid lineage and is associated with foraging specialization and increased ecological success. We examined the developmental and genetic origins for this phenotype and found that the snout is composed of two hypertrophied tissues: the intermaxillary ligament (IML), which connects the right and left sides of the upper jaw, and the overlying loose connective tissue. The IML is present in all cichlids, but in its exaggerated form it interdigitates with the more superficial connective tissue and anchors to the epithelium, forming a unique ligament–epithelial complex. We examined the Transforming growth factor β (Tgfβ) → Scleraxis (Scx) candidate pathway and confirmed a role for these factors in snout development. We demonstrate further that experimental up-regulation of Tgfβ is sufficient to produce an expansion of scx expression and concomitant changes in snout morphology. Genetic and genomic mapping show that core members of canonical Tgfβ signaling segregate with quantitative trait loci (QTL) for snout variation. These data also implicate a candidate for ligament development, adam12, which we confirm using the zebrafish model. Collectively, these data provide insights into ligament morphogenesis, as well as how an ecologically relevant novelty can arise at the molecular level.