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Legan, A. W.

Publications and source records attributed to Legan, A. W..

6 recordsLinked to original sources

Lineage-specific patterns of sexually dimorphic antennal transcription in the paper wasp Polistes fuscatus

Olfaction mediates many behaviors in social Hymenoptera, with sexual dimorphism in antennal transcription associated with different behaviors between sexes. Females display coordinated social behaviors within colonies, while males exhibit limited social behavior but are selected for finding mates. The expanded "9-exon" odorant receptor (OR) gene subfamily is associated with chemical communication and exhibits strongly female biased antennal transcription in ants and honey bees. Polistine wasps represent an independent evolution of sociality and associated expansion of 9-exon ORs, though antennal expression patterns are unknown. Here, we report distinct patterns of sexually dimorphic OR transcription in Polistes fuscatus compared to ants and bees. Most P. fuscatus 9-exon transcripts were detected at similar levels in males and females, and some were male biased. We also report differential antennal transcription of cytochromes P450 and muscle-related genes between sexes. We discuss these patterns in the context of the unique sexual and social behaviors of Polistes wasps, including prolonged male mating aggregations and male antennal tapping and curling during courtship and copulation. These results call attention to the lineage-specific selective pressures shaping sexually dimorphic antennal transcription in social insects.

evolutionary biology↗

Postural analysis reveals persistent vigilance in paper wasps after conspecific challenge

Vigilant animals detect and respond to threats in the environment, often changing posture and movement patterns. In social animals vigilance is modulated not only by predators but also by threatening conspecifics. Precisely how social interactions alter vigilance behavior over time is not well understood. We report persistent effects of a simulated social challenge on the vigilance behavior of wild northern paper wasp foundresses, Polistes fuscatus. During the founding phase of the colony cycle conspecific wasps may usurp nests from the resident foundress, representing a severe threat. Using postural tracking, we found that after simulated intrusions wasps displayed increased vigilance during the minutes after the threat was removed. Sustained vigilance elicited after social threat manifested as increased movement, greater bilateral wing extension, and reduced antennal separation. However, no postural changes were observed after a control stimulus presentation. By rapidly adjusting individual vigilance behavior after fending off a conspecific intruder, paper wasp foundresses invest in surveillance of potential social threats, even when such threats are no longer immediately present. The prolonged state of vigilance observed here is relevant to plasticity of recognition processes as a result of conspecific threats.

animal behavior and cognition↗

First record of anti-predator behavior in the gall-forming aphid Mordwilkoja vagabunda

The gall-forming aphid Mordwilkoja vagabunda has been an outgroup in molecular studies of the evolution of social behavior in the Pemphigus genus, but Mordwilkoja aphids have not previously been assayed for social behavior, such as altruistic defense. This study reports experiments carried out in July in Ithaca, NY, USA, in which nymphs (immature aphids) of M. vagabunda were video recorded under a stereo microscope while they encountered pyralid moth larvae in a plastic arena. M. vagabunda nymphs of all instars used their legs to claw moth larvae while pressing their rostrums against the larvae, possibly to pierce the cuticle. Many of the attacking aphids were alatoid nymphs, rather than the specialized first instar soldiers typically observed in Pemphigus species. M. vagabunda nymphs moved in bursts that sometimes became synchronized among several aphids in the same vicinity. These synchronized, rhythmic movements may be anti-predator defense strategies comparable to the collective twitching and kicking response observed in colonies of Aphis nerii and other aphid species. Defensive behaviors by M. vagabunda nymphs may be altruistic fortress defense strategies which maximize inclusive fitness of the clone. Open Research statementVideo data are shared publicly on a repository, Zenodo, at this DOI: https://doi.org/10.5281/zenodo.5636845

animal behavior and cognition↗

Evidence for a selective link between cooperation and individual recognition

The ability to recognize and discriminate among others is a frequent assumption of models of the evolution of cooperative behavior. At the same time, cooperative behavior has been proposed as a selective agent favoring the evolution of individual recognition abilities. While theory predicts that recognition and cooperation may co-evolve, data linking recognition abilities and cooperative behavior with fitness or evidence of selection are elusive. Here, we provide evidence of a fitness link between individual recognition and cooperation in the paper wasp Polistes fuscatus. Nest founding females in northern populations frequently form cooperative multiple foundress nests and possess highly variable facial patterns that mediate individual recognition. We describe a dearth of cooperative nesting, low phenotypic diversity, and a lack of individual recognition in southern populations. In a common garden experiment, northern co-foundress associations successfully reared offspring while all cooperative southern groups failed to rear any offspring, suggesting a fitness link between individual recognition and successful cooperation. Consistent with a selective link between individual recognition and cooperation, we find that rates of cooperative co-nesting correlate with identity-signaling color pattern diversity across the species range. Moreover, genomic evidence of recent positive selection on cognition loci likely to mediate individual recognition is substantially stronger in northern compared to southern P. fuscatus populations. Collectively, these data suggest that individual recognition and cooperative nesting behavior have co-evolved in P. fuscatus because recognition helps mediate conflict among co-nesting foundresses. This work provides evidence of a specific cognitive phenotype under selection because of social interactions, supporting the idea that social behavior can be a key driver of cognitive evolution.

animal behavior and cognition↗

Expansion and accelerated evolution of 9-exon odorant receptors in Polistes paper wasps (Hymenoptera: Vespidae)

Independent origins of sociality in bees and ants are associated with independent expansions of particular odorant receptor (OR) gene subfamilies. In ants, one clade within the OR gene family, the 9-exon subfamily, has dramatically expanded. These receptors detect cuticular hydrocarbons (CHCs), key social signaling molecules in insects. It is unclear to what extent 9-exon OR subfamily expansion is associated with the independent evolution of sociality across Hymenoptera, warranting studies of taxa with independently derived social behavior. Here we describe odorant receptor gene family evolution in the northern paper wasp, Polistes fuscatus, and compare it to four additional paper wasp species spanning ~40 million years of divergence. We find 200 functional OR genes in P. fuscatus matching predictions from neuroanatomy, and more than half of these are in the 9-exon subfamily. Lineage-specific expansions of 9-exon subfamily ORs are tandemly arrayed in Polistes genomes and exhibit a breakdown in microsynteny relative to tandem arrays in other OR subfamilies. There is evidence of episodic positive diversifying selection shaping ORs in expanded subfamilies, including 9-exon, E, H, and L, but 9-exon ORs do not stand out as selectively diversified among Polistes species. Accelerated evolution has resulted in lower amino acid similarity and high dN/dS among 9-exon ORs compared to other OR subfamilies. Patterns of OR evolution within Polistes are consistent with 9-exon OR function in CHC perception by combinatorial coding, with both selection and drift contributing to interspecies differences in copy number and sequence.

evolutionary biology↗

Evolutionary dynamics of recent selection for enhanced social cognition

Cognitive abilities can vary dramatically among species though little is known about the dynamics of cognitive evolution. Here we demonstrate that recent evolution of visual individual recognition in the paper wasp Polistes fuscatus is the target of arguably the strongest positive selective pressure in the species recent history. The most extreme selective sweeps in P. fuscatus are associated with genes known to be involved in long-term memory formation, mushroom body development and visual processing - all traits that have recently evolved in association with individual recognition. Cognitive evolution appears to have been driven initially by selection on standing variation in perceptual traits followed by both hard and soft sweeps on learning and memory. Evolutionary modeling reveals that intense selection as observed in P. fuscatus is likely the norm during the early stages of cognitive evolution. These data provide insight into the dynamics of cognition evolution demonstrating that social selection for increased intelligence can lead to rapid multi-genic adaptation of enhanced recognition abilities.

animal behavior and cognition↗