James H. Hunt

Multigene phylogeny reveals eusociality evolved twice in vespid wasps

Eusocial wasps of the family Vespidae are thought to have derived their social behavior from a common ancestor that had a rudimentary caste-containing social system. In support of this behavioral scenario, the leading phylogenetic hypothesis of Vespidae places the eusocial wasps (subfamilies Stenogastrinae, Polistinae, and Vespinae) as a derived monophyletic clade, thus implying a single origin of eusocial behavior. This perspective has shaped the investigation and interpretation of vespid social evolution for more than two decades. Here we report a phylogeny of Vespidae based on data from four nuclear gene fragments (18S and 28S ribosomal DNA, abdominal-A and RNA polymerase II) and representatives from all six extant subfamilies. In contrast to the current phylogenetic perspective, our results indicate two independent origins of vespid eusociality, once in the clade Polistinae+Vespinae and once in the Stenogastrinae. The stenogastrines appear as an early diverging clade distantly related to the vespines and polistines and thus evolved their distinctive form of social behavior from a different ancestor than that of Polistinae+Vespinae. These results support earlier views based on life history and behavior and have important implications for interpreting transitional stages in vespid social evolution.

A diapause pathway underlies the gyne phenotype in Polistes wasps, revealing an evolutionary route to caste-containing insect societies.

Colonies of social wasps, ants, and bees are characterized by the production of two phenotypes of female offspring, workers that remain at their natal nest and nonworkers that are potential colony reproductives of the next generation. The phenotype difference includes morphology and is fixed during larval development in ants, honey bees, and some social wasps, all of which represent an advanced state of sociality. Paper wasps (Polistes) lack morphological castes and are thought to more closely resemble an ancestral state of sociality wherein the phenotype difference between workers and nonworkers is established only during adult life. We address an alternative hypothesis: a bias toward the potential reproductive (gyne) phenotype among Polistes female offspring occurs during larval development and is based on a facultatively expressed ancestral life history trait: diapause. We show that two signatures of diapause (extended maturation time and enhanced synthesis and sequestration of a hexameric storage protein) characterize the development of gyne offspring in Polistes metricus. Hexameric storage proteins are implicated in silencing juvenile hormone signaling, which is a prerequisite for diapause. Diverging hexamerin protein dynamics driven by changes in larval provisioning levels thereby provide one possible mechanism that can cause an adaptive shift in phenotype bias during the Polistes colony cycle. This ontogenetic basis for alternative female phenotypes in Polistes challenges the view that workers and gynes represent behavior options equally available to every female offspring, and it exemplifies how social insect castes can evolve from casteless lineages.

Lipid stores, ovary development, and brain gene expression in Polistes metricus females

Abstract.In order to gain insights into the mechanistic basis of caste and behavioral differences in Polistes paper wasps, we examined abdominal lipid stores and ovary development in Polistes metricus females in four groups: foundresses, queens, workers, and gynes. Queens had the largest ovaries, followed by foundresses, workers, and gynes. Gynes had 6x higher lipid stores than the other groups, and lipid stores were lower in foragers (foundresses, workers) than non-foragers (queens, gynes). Lipid levels and ovary development were negatively correlated across the four groups, but removing gynes from the analysis revealed a significant positive correlation for foundresses, workers, and queens, suggesting different energy allocation strategies for gynes vs. other groups. Expression levels of 9 genes (including three in the insulin pathway), examined in a previous study, correlated with either lipid stores or ovary development. These correlative results suggest important relationships between nutrition, reproduction, and division of labor in primitively social insects. We also show that it is possible to assign P. metricus females to one of the four female groups on the basis of wing wear (an indicator of foraging experience), lipid stores, and ovary development, which can facilitate caste-specific collections for future studies.

Storage proteins in vespid wasps: characterization, developmental pattern, and occurrence in adults

Wasps of family Vespidae contain three types of major proteins that have the size, amino acid composition, subunit composition, immunological reactivity, and pattern of occurrence characteristic of storage proteins. The three types of storage protein, which have been identified in other Hymenoptera, are very high density lipoprotein, high glutamine/glutamic acid protein, and hexamerin. The predominant pattern of occurrence for these proteins is as known from most or all Holometabola: synthesis during the last larval instar and utilization as an amino acid source during metamorphosis. Hexamerin also occurred in a large young adult female Monobia quadridens but not a small one, which suggests that carry-over into adult females is a reaction norm response to quantity of larval provisions, because these wasps could not have fed as adults. In two paper wasp species of the genus Polistes, hexamerin was present in large adult females which emerged during the colony cycle phase when reproductive females are typically produced, but not in adult female offspring that emerged earlier in the colony cycle or in adult females that were workers. It cannot be confirmed by these data that the hexamerin in the adult paper wasps represented carry-over from metamorphosis rather than post-emergence feeding, but the pattern of occurrence suggests that presence of storage protein may play a role in caste differentiation in paper wasps. No storage protein was found in any adult Vespula maculifrons, a yellowjacket wasp, suggesting that caste differentiation in vespine wasps does not incorporate storage protein as a component.

Differential gene expression and protein abundance evince ontogenetic bias toward castes in a primitively eusocial wasp.

Polistes paper wasps are models for understanding conditions that may have characterized the origin of worker and queen castes and, therefore, the origin of paper wasp sociality. Polistes is “primitively eusocial” by virtue of having context-dependent caste determination and no morphological differences between castes. Even so, Polistes colonies have a temporal pattern in which most female larvae reared by the foundress become workers, and most reared by workers become future-reproductive gynes. This pattern is hypothesized to reflect development onto two pathways, which may utilize mechanisms that regulate diapause in other insects. Using expressed sequence tags (ESTs) for Polistes metricus we selected candidate genes differentially expressed in other insects in three categories: 1) diapause vs. non-diapause phenotypes and/or worker vs. queen differentiation, 2) behavioral subcastes of worker honey bees, and 3) no a priori expectation of a role in worker/gyne development. We also used a non-targeted proteomics screen to test for peptide/protein abundance differences that could reflect larval developmental divergence. We found that foundress-reared larvae (putative worker-destined) and worker-reared larvae (putative gyne-destined) differed in quantitative expression of sixteen genes, twelve of which were associated with caste and/or diapause in other insects, and they also differed in abundance of nine peptides/proteins. Some differentially-expressed genes are involved in diapause regulation in other insects, and other differentially-expressed genes and proteins are involved in the insulin signaling pathway, nutrient metabolism, and caste determination in highly social bees. Differential expression of a gene and a peptide encoding hexameric storage proteins is especially noteworthy. Although not conclusive, our results support hypotheses of 1) larval developmental pathway divergence that can lead to caste bias in adults and 2) nutritional differences as the foundation of the pathway divergence. Finally, the differential expression in Polistes larvae of genes and proteins also differentially expressed during queen vs. worker caste development in honey bees may indicate that regulatory mechanisms of caste outcomes share similarities between primitively eusocial and advanced eusocial Hymenoptera.

Intracolony chemical communication in social insects

Chemical messengers are the primary mode of intracolony communication in the majority of social insect species. Chemically transmitted information plays a major role in nestmate recognition and kin recognition. Physical and behavioral castes often differ in chemical signature, and queen effects can be significant regulators of behavior and reproduction. Chemical messengers themselves differ in molecular structure, and the effects on behavior and other variables can differ as a consequence of not only molecular structure of the chemical messenger itself but also of its temporal expression, quantity, chemical blends with other compounds, and effects of the environment. The most studied, and probably the most widespread, intracolony chemical messengers are cuticular hydrocarbons (CHCs). CHCs are diverse and have been well studied in social insects with regard to both chemical structure and their role as pheromones. CHCs and other chemical messengers can be distributed among colony members via physical contact, grooming, trophallaxis, and contact with the nesting substrate. Widespread intracolony distribution of chemical messengers gives each colony a specific odor whereby colony members are integrated into the social life of the colony and non-members of the colony are excluded. Colony odor can vary as a function of genetic diversity within the colony, and the odor of a colony can change as a function of colony age and environmental effects. Chemical messengers can disseminate information on the presence of reproductives and fertility of the queen(s) and workers, and queen pheromone can play a significant role in suppressing reproduction by other colony members. New analytical tools and new avenues of investigation can continue to expand knowledge of how individual insects function as members of a society and how the society functions as a collective.

Food Quantity Affects Traits of Offspring in the Paper Wasp Polistes metricus (Hymenoptera: Vespidae)

Abstract The effects of food quantity on the morphology and development of the paper wasp Polistes metricus Say are studied, and experimental results are compared with predictions of the parental manipulation hypothesis. Food deprivation led to smaller female offspring. By hand feeding larvae we used a technique that counteracts the queen’s hypothesized ability to restrict food provisioning. Hand feeding larvae did not result in larger offspring, but their abdomen was wider and heavier and the hand-fed wasps survived longer in a cold test. We infer that hand-fed colonies produced more gynes and fewer workers than did control colonies. Results of a restricted nourishment treatment do not support the differential feeding hypothesis, because in fasting colonies the emergence of all larvae was delayed by a month, and we did not detect discriminatory feeding of particular larvae for faster emergence. Although fasting colonies produced fewer offspring, the sex ratio did not show significant differences from the other groups. These data suggest that Polistes metricus colonies are partly able to respond to different nutritional conditions by allocating excess food to increase the number of gynes at the expense of workers.

A conceptual model for the origin of worker behaviour and adaptation of eusociality.

In a model based on the wasp family Vespidae, the origin of worker behaviour, which constitutes the eusociality threshold, is not based on relatedness, therefore the origin of eusociality does not depend on inclusive fitness, and workers at the eusociality threshold are not altruistic. Instead, incipient workers and queens behave selfishly and are subject to direct natural selection. Beyond the eusociality threshold, relatedness enables ‘soft inheritance’ as the framework for initial adaptations of eusociality. At the threshold of irreversibility, queen and worker castes become fixed in advanced eusociality. Transitions from solitary to facultative, facultative to primitive, and primitive to advanced eusociality occur via exaptation, phenotypic accommodation and genetic assimilation. Multilevel selection characterizes the solitary to highly eusocial transition, but components of multilevel selection vary across levels of eusociality. Roles of behavioural flexibility and developmental plasticity in the evolutionary process equal or exceed those of genotype.

Observations onApoica pallens, a nocturnal neotropical social wasp (Hymenoptera: Vespidae, Polistinae, Epiponini)

SummaryColonies and nests ofApoica pallens in the llanos region of Venezuela range from small foundress nests to large mature colonies. Nests are sited on small diameter, near-horizontal branches in a variety of shrub and tree species. During the day, adult wasps cluster on the face of the nest in an array that seems to be determined by orientation to gravity; defense of the colony against parasitoids and ants by the resting wasps may be more a passive than an active behavior. Wasps fan their wings to cool the colony during the day, but no foraging for water accompanies the fanning behavior. Nightly foraging activity begins with the explosive departure from the nest of hundreds of wasps, most of which rapidly return. Moderate foraging levels early at night give way to very low foraging levels in pre-dawn hours. The period of moderate foraging may be extended for longer hours during increased moonlight. Foraging wasps collect arthropod provisions for larvae. Larvae produce a trophallactic saliva; adults engage in inter-adult trophallaxis; brood are cannibalized. During cluster formation prior to swarm emigration, adult wasps do not appear to scent-mark substrates such as leaves. Instead,A. pallens exhibits a calling behavior, unique among polistine wasps studied to date, in which the gaster is held rigidly away from the thorax and metasomal sternal glands are exposed. Swarms can emigrate during the day.A. pallens may incorporate absconding and colony relocation as features of its colony cycle in the highly seasonal llanos.

Intracolony vibroacoustic communication in social insects

Vibrations and sounds, collectively called vibroacoustics, play significant roles in intracolony communication in termites, social wasps, ants, and social bees. Modalities of vibroacoustic signal production include stridulation, gross body movements, wing movements, high-frequency muscle contractions without wing movements, and scraping mandibles or tapping body parts on resonant substrates. Vibroacoustic signals are perceived primarily via Johnston’s organs in the antennae and subgenual organs in the legs. Substrate vibrations predominate as vibroacoustic modalities, with only honey bees having been shown to be able to hear airborne sound. Vibroacoustic messages include alarm, recruitment, colony activation, larval provisioning cues, and food resource assessment. This review describes the modalities and their behavioral contexts rather than electrophysiological aspects, therefore placing emphasis on the adaptive roles of vibroacoustic communication. Although much vibroacoustics research has been done, numerous opportunities exist for continuations and new directions in vibroacoustics research.