Biology subjects

Sheehan, M. J.

Publications and source records attributed to Sheehan, M. J..

27 records · Page 2Linked to original sources

bioRxiv2021

Color is necessary for specialized face learning in the Northern paper wasp, Polistes fuscatus

Visual individual recognition requires animals to distinguish among conspecifics based on appearance. Though visual individual recognition has been reported in a range of taxa, the features that animals rely on to discriminate between individuals are often not well understood. Northern paper wasp females, Polistes fuscatus, possess individually distinctive color patterns on their faces, which mediate individual recognition. It is currently unclear what facial features P. fuscatus use to distinguish individuals. The anterior optic tubercle, a chromatic processing brain region, is especially sensitive to social experience during development, suggesting that color may be important for recognition in this species. We sought to test the roles of color in wasp facial recognition. Color may be important simply because it creates a pattern. If this is the case, then wasps should perform similarly when discriminating color or grayscale images of the same faces. Alternatively, color itself may be important for recognition, which would predict poorer performance on grayscale image discrimination relative to color images. We found wasps trained on grayscale faces, unlike those trained on color images, did not perform better than chance. Suggesting that color is necessary for the recognition of an image as a face by the wasp visual system.

animal behavior and cognition↗

bioRxiv2021

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↗

bioRxiv2021

Sex differences in deleterious genetic variants in a haplodiploid social insect

Deleterious variants are selected against but can linger in populations at low frequencies for long periods of time, decreasing fitness and contributing to disease burden in humans and other species. Deleterious variants occur at low frequency but distinguishing deleterious variants from low frequency neutral variation is challenging based on population genetics data. As a result, we have little sense of the number and identity of deleterious variants in wild populations. For haplodiploid species, it has been hypothesized that deleterious alleles will be directly exposed to selection in haploid males, but selection can be masked in diploid females due to partial or complete dominance, resulting in more efficient purging of deleterious mutations in males. Therefore, comparisons of the differences between haploid and diploid genomes from the same population may be a useful method for inferring rare deleterious variants. This study provides the first formal test of this hypothesis. Using wild populations of Northern paper wasps (Polistes fuscatus), we find that males have fewer overall variants, and specifically fewer missense and nonsense variants, than females from the same population. Allele frequency differences are especially pronounced for rare missense and nonsense mutations and these differences lead to a lower genetic load in males than females. Based on these data we estimate that a large number of highly deleterious mutations are segregating in the paper wasp population. Stronger selection against deleterious alleles in haploid males may have implications for adaptation in other haplodiploid insects and provides evidence that wild populations harbor abundant deleterious variants.

evolutionary biology↗

bioRxiv2021

Dynamic neurogenomic responses to social interactions and dominance outcomes in female paper wasps

Social interactions have large effects on individual physiology and fitness. In the immediate sense, social stimuli are often highly salient and engaging. Over longer time scales, competitive interactions often lead to distinct social ranks and differences in physiology and behavior. Understanding how initial responses lead to longer-term effects of social interactions requires examining the changes in responses over time. Here we examined the effects of social interactions on transcriptomic signatures at two points, at the end of a 45-minute interaction and 4 hours later, in female Polistes fuscatus paper wasp foundresses. Female P. fuscatus have variable facial patterns that are used for visual individual recognition, so we separately examined the transcriptional dynamics in the optic lobe and the central brain. Results demonstrate much stronger transcriptional responses to social interactions in the central brain compared to the optic lobe. Differentially regulated genes in response to social interactions are enriched for memory-related transcripts. Comparisons between winners and losers of the encounters revealed similar overall transcriptional profiles at the end of an interaction, which significantly diverged over the course of 4 hours, with losers showing changes in expression levels of genes associated with aggression and reproduction in paper wasps. On nests, subordinate foundresses are less aggressive, do more foraging and lay fewer eggs compared to dominant foundresses and we find losers shift expression of many genes, including vitellogenin, related to aggression, worker behavior, and reproduction within hours of losing an encounter. These results highlight the early neurogenomic changes that likely contribute to behavioral and physiological effects of social status changes in a social insect.

genomics↗

bioRxiv2020

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↗

bioRxiv2019

Distinct evolutionary trajectories of V1R clades across mouse species

BackgroundMany animals rely heavily on olfaction to navigate their environment. Among rodents, olfaction is crucial for a wide range of social behaviors. The vomeronasal olfactory system in particular plays an important role in mediating social communication, including the detection of pheromones and recognition signals. Currently, very few vomeronasal receptors have known ligands, which severely limits our understanding of chemosensory-driven social communication. In this study we examine patterns of vomeronasal type-1 receptor (V1R) evolution in the house mouse and related species within the genus Mus. By exploring the evolution of these receptors, we provide insight into the functional roles of receptor subtypes as well as the dynamics of gene family evolution. ResultsWe generated transcriptomes from the vomeronasal organs of 5 Mus species, and produced high quality V1R repertoires for each species. We find that V1R clades in the house mouse and relatives exhibit distinct evolutionary trajectories. Some clades are highly conserved, while others reveal patterns of rapid evolutionary change. We identify putative species-specific gene expansions, including a dramatic clade D expansion in the house mouse. While gene gains are abundant, we detect very few gene losses. We describe a novel V1R clade and highlight candidate receptors for future de-orphanization. Based on clade-level evolutionary patterns, we identify receptor families that are strong candidates for detecting social signals and predator cues. Our results further support the view that V1Rs are important for detecting the physiological status of conspecifics, particularly female estrus cues. ConclusionAnalysis of clade-level evolution is critical for understanding species chemosensory adaptations. This study provides clear evidence that V1R clades are characterized by distinct evolutionary trajectories. As receptor evolution is shaped by ligand identity, these results provide a framework for examining the functional roles of different receptors.

evolutionary biology↗

bioRxiv2019

RAD-Behavior (Recombining Atomized, Discretized, Behavior): A new framework for the quantitative analysis of behavioral execution

The ability to precisely describe and numerically evaluate organismal phenotypes is a prerequisite for addressing most questions in evolutionary biology and ecology. The quantification and comparison of behavior, loosely defined as an external response to stimuli, is particularly challenging because the myriad axes of variation that exist make comparisons, both within and among species, difficult. Such evaluations often boil down to comparisons of time-budgets (e.g. relative investment in courtship displays) or probabilities (e.g. likelihood of engaging in a class of behaviors in a particular context) - which we refer to as behavioral strategies. A focus on variation in behavioral strategies underlies most research in evolutionary and ecological studies of behavior. Equally important, however, is perhaps the question of how animals are actually performing the complex motor sequences that comprise behaviors (i.e. behavioral execution). What are the patterns of movement, the relative transition rates, and kinematics underlying the behaviors exhibited in particular contexts? Understanding how behavioral execution differs among individuals, populations, and species has the potential to provide new insights into the factors shaping variation in behavior and the processes shaping behavioral evolution at different scales. Here, we propose a broad framework for comparing behavioral execution (RAD-behavior: recombining atomized, discretized behavior) that leverages string-matching/bioinformatic tools to understand phenotypic variation in behavioral execution and which holds the potential to yield novel insights about the evolutionary ecology of behavior at multiple scales.

animal behavior and cognition↗

bioRxiv2019

The giant pouched rat (Cricetomys ansorgei) olfactory receptor repertoire

For rodents, olfaction is essential for locating food, recognizing mates and competitors, avoiding predators, and navigating their environment. It is thought that rodents may have expanded olfactory receptor repertoires in order to specialize in olfactory behavior. Despite being the largest clade of mammals and depending on olfaction relatively little work has documented olfactory repertoires outside of the conventional laboratory mice and rats. Here we report the olfactory receptor repertoire of the African giant pouched rat (Cricetomys ansorgei), a Muroid rodent distantly related to mice and rats. The African giant pouched rat is notable for its large cortex and olfactory bulbs relative to its body size compared to other sympatric rodents, which suggests anatomical elaboration of olfactory capabilities. We hypothesized that in addition to anatomical elaboration for olfaction, these pouched rats might also have an expanded olfactory receptor repertoire to enable their olfactory behavior. We examined the composition of the olfactory receptor repertoire to better understand how their sensory capabilities have evolved. We identified 1145 functional olfactory genes, and 260 additional pseudogenes within 301 subfamilies from the African giant pouched rat genome. This repertoire is similar to mice and rats in terms of size, pseudogene percentage and number of subfamilies. Analyses of olfactory receptor gene trees revealed that the pouched rat has 6 expansions in different subfamilies compared to mice, rats and squirrels. We identified 99 orthologous genes conserved among 4 rodent species and an additional 167 conserved genes within the Muroid rodents. The orthologous genes shared within Muroidea suggests that there may be a conserved Muroid-specific olfactory receptor repertoire. We also note that the description of this repertoire can serve as a complement to other studies of rodent olfaction, as the pouched rat is an outgroup within Muroidea. Thus, our data suggest that African giant pouched rats are capable of both natural and trained olfactory behaviors with a typical Muriod olfactory receptor repertoire.

evolutionary biology↗

bioRxiv2018

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↗