Biology subjects

Tumulty, J. P.

Publications and source records attributed to Tumulty, J. P..

5 recordsLinked to original sources

bioRxiv2022

Co-option of ancestral signal elements in the evolution of a cooperative parental behavior

The emergence of complex social interactions is predicted to be an important selective force in the diversification of communication systems. Parental care presents a key social context in which to study the evolution of novel signals, as care often requires communication and behavioral coordination between parents and is an evolutionary stepping-stone towards increasingly complex social systems. Anuran amphibians (frogs and toads) are a classic model of acoustic communication and the vocal repertoires of many species have been characterized in the contexts of advertisement, courtship, and aggression; yet quantitative descriptions of calls elicited in the context of parental care are lacking. The biparental poison frog, Ranitomeya imitator, exhibits a remarkable parenting behavior in which females, cued by the calls of their male partners, feed tadpoles unfertilized eggs. Here, we characterized and compared calls across three social contexts, for the first time including a parental care context. We found that egg feeding calls share some properties with both advertisement and courtship calls but also had unique properties. Multivariate analysis revealed high classification success for advertisement and courtship calls but misclassified nearly half of egg feeding calls as either advertisement or courtship calls, suggesting additional signal modalities play a role in parental communication. Egg feeding and courtship calls both contained less identity information than advertisement calls, as expected for signals used in close-range communication where uncertainty about identity is low. Taken together, egg feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response. Significance StatementParental care has evolved independently in every major animal lineage and represents a major step in the evolution of complex sociality. Communication systems may need to increase in complexity. To explore these ideas, we characterized calls associated with trophic egg feeding, a unique cooperative parental behavior in the biparental mimic poison frog and compared them to calls associated with mate attraction (advertisement and courtship calls). Our analysis revealed some distinct, but many shared properties of signals elicited during egg feeding, suggesting that signals deployed in a novel social context evolve via modification and recombination of existing signals. These findings deepen our understanding of the relationship between complexity of social and communication systems.

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

Predicting and measuring decision rules for social recognition in a Neotropical frog

Many animals use signals, such as vocalizations, to recognize familiar individuals. However, animals risk making recognition mistakes because the signal properties of different individuals often overlap due to within-individual variation in signal production. To understand the relationship between signal variation and decision rules for social recognition, we studied male golden rocket frogs, which recognize the calls of territory neighbors and respond less aggressively to a neighbors calls than to the calls of strangers. We quantified patterns of individual variation in acoustic properties of calls and predicted optimal discrimination thresholds using a signal detection theory model of receiver utility that incorporated signal variation, the payoffs of correct and incorrect decisions, and the rates of encounters with neighbors and strangers. We then experimentally determined thresholds for discriminating between neighbors and strangers using a habituation-discrimination experiment with territorial males in the field. Males required a threshold difference between 9% and 12% to discriminate between calls differing in temporal properties; this threshold matched those predicted by a signal detection theory model under ecologically realistic assumptions of infrequent encounters with strangers and relatively costly missed detections of strangers. We demonstrate empirically that receivers group continuous variation in vocalizations into discrete social categories and show that signal detection theory can be applied to investigate evolved decision rules.

animal behavior and cognition↗

bioRxiv2021

Identity signaling, identity reception and the evolution of social recognition in a Neotropical frog

Animals recognize familiar individuals to perform a variety of important social behaviors. Social recognition is often mediated by communication between signalers who produce signals that contain identity information and receivers who categorize these signals based on previous experience. We tested two hypotheses about adaptations in signalers and receivers that enable the evolution of social recognition using two species of closely related territorial poison frogs. Male golden rocket frogs (Anomaloglossus beebei) recognize the advertisement calls of conspecific territory neighbors and display a "dear enemy effect" by responding less aggressively to neighbors than strangers, while male Kai rocket frogs (A. kaiei) do not. Our results did not support the identity signaling hypothesis: both species produced advertisement calls that contain similar amounts of identity information. Our results did support the identity reception hypothesis: both species exhibited habituation of aggression to playbacks simulating the arrival of a new neighbor, but only golden rocket frogs showed renewed aggression when they subsequently heard calls from a different male. These results suggest that an ancestral mechanism of plasticity in aggression common among frogs has been modified through natural selection to be specific to calls of individual males in golden rocket frogs, enabling a social recognition system.

animal behavior and cognition↗

bioRxiv2020

Ecological and social drivers of neighbor recognition and the dear enemy effect in a poison frog

Navigating social relationships frequently rests on the ability to recognize familiar individuals using phenotypic characteristics. Across diverse taxa, animals vary in their capacities for social recognition but the ecological and social sources of selection for recognition are often unclear. In a comparative study of two closely related species of poison frogs, we identified a species difference in social recognition of territory neighbors and investigated potential sources of selection underlying this difference. In response to acoustic playbacks, male golden rocket frogs (Anomaloglossus beebei) recognized the calls of neighbors and displayed a "dear enemy effect" by responding less aggressively to neighbors calls than strangers calls. In contrast, male Kai rocket frogs (Anomaloglossus kaiei) were equally aggressive to the calls of neighbors and strangers. This species difference in behavior was associated with key differences in reproductive ecology and characteristics of territories. Golden rocket frogs defended reproductive resources in the form of bromeliads, which is expected to create a threat asymmetry between neighbors and strangers favoring decreased aggression to neighbors. In contrast, Kai rocket frogs did not defend reproductive resources. Further, compared with Kai rocket frog territories, golden rocket frog territories occurred at higher densities and were defended for longer periods of time, creating a more complex social environment with more opportunities for repeated but unnecessary aggression between neighbors, which should favor the ability to recognize and exhibit less aggression towards neighbors. These results suggest that differences in reproductive ecology can drive changes in social structure that select for social recognition.

animal behavior and cognition↗