Evidence for a selective link between cooperation and individual recognition.

The ability to recognize others is a frequent assumption of models of the evolution of cooperation. At the same time, cooperative behavior has been proposed as a selective agent favoring the evolution of individual recognition abilities. Although theory predicts that recognition and cooperation may co-evolve, data linking recognition abilities and cooperative behavior with evidence of selection are elusive. Here, we provide evidence of a selective link between individual recognition and cooperation in the paper wasp Polistes fuscatus through a combination of clinal, common garden, and population genomics analyses. We identified latitudinal clines in both rates of cooperative nesting and color pattern diversity, consistent with a selective link between recognition and cooperation. In behavioral experiments, we replicated previous results demonstrating individual recognition in cooperative and phenotypically diverse P. fuscatus from New York. In contrast, wasps from a less cooperative and phenotypically uniform Louisiana population showed no evidence of individual recognition. In a common garden experiment, groups of wasps from northern populations formed more stable and individually biased associations, indicating that recognition facilitates group stability. The strength of recent positive selection on cognition-associated loci likely to mediate individual recognition is substantially greater in northern compared with southern P. fuscatus populations. Collectively, these data suggest that individual recognition and cooperative nesting behavior have co-evolved in P. fuscatus because recognition helps stabilize social groups. 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.

Evolution of acoustic signals associated with cooperative parental behavior in a poison frog.

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 toward 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. 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 and additional signal modalities may be used. Taken together, egg-feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response.

Predicting and Measuring Decision Rules for Social Recognition in a Neotropical Frog.

AbstractMany animals use signals to recognize familiar individuals but risk making mistakes because the signal properties of different individuals often overlap. Furthermore, outcomes of correct and incorrect decisions yield different fitness payoffs, and animals incur these payoffs at different frequencies depending on interaction rates. To understand how signal variation, payoffs, and interaction rates shape recognition decision rules, we studied male golden rocket frogs, which recognize the calls of territory neighbors and are less aggressive to neighbors than to strangers. We first quantified patterns of individual variation in call properties and predicted optimal discrimination thresholds using signal variation. We then measured thresholds for discriminating between neighbors and strangers using a habituation-discrimination field playback experiment. Territorial males discriminated between calls differing by 9%-12% in temporal properties, slightly higher than the predicted thresholds (5%-10%). Finally, we used a signal detection theory model to explore payoff and interaction rate parameters and found that the empirical threshold matched those predicted under ecologically realistic assumptions of infrequent encounters with strangers and relatively costly missed detections of strangers. We demonstrate that receivers group continuous variation in vocalizations into discrete social categories and that signal detection theory can be applied to understand evolved decision rules.

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, whereas male Kai rocket frogs (Anomaloglossus 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 missing from data archives.

An investigation into animal behavior data archiving practices revealed low rates of data archiving, frequent issues with archived data, and a near absence of multimedia data from data archives. Increasing archiving of animal behavior data will improve the integrity of current studies and enable new avenues of research.

Hormonal modulation of reproduction in Polistes fuscatus social wasps: Dual functions in both ovary development and sexual receptivity.

Hormones are often major regulators of complex behaviors, such as mating and reproduction. In insects, juvenile hormone (JH) is integral to many components of reproductive physiology and behavior, but its role in female sexual receptivity is not well understood. To investigate the influence of JH on receptivity, we utilized the social wasp Polistes fuscatus. In Polistes, mating behavior is temporally separated from other components of reproduction, which allows for examination of the physiology and behavior of mating, disentangled from fertilization and egg-laying. We reared virgin gynes (reproductive females) in the lab and divided them into four groups, in which gynes received multiple topical treatments of either 20 µg, 10 µg, 5 µg, or 0 µg of the JH analog methoprene. Gynes were then placed in petri dishes with 2 unrelated males and we recorded attempted and successful mating. Additionally, we measured gyne ovarian development and survival in each group. We found that methoprene increased both sexual receptivity and ovarian development, but was associated with a decrease in long-term survival. Receptivity increased linearly as methoprene treatment increased, but the effect of methoprene on ovarian development was independent of dose. These results demonstrate the importance of JH in sexual receptivity and mating behavior. We argue that the relatively understudied Polistes gyne has potential as a model for mating and reproduction, and for the internal and external regulation of this complex behavior.

Plant-borne vibrations modulate calling behaviour in a tropical amphibian.

Terrestrial frogs and toads produce conspicuous vocalizations that may be accompanied by substrate-borne vibrations [1]. Unlike airborne sound, these substrate-borne components are relatively understudied in animal communication. Some anurans exploit the forest floor as a relatively noiseless communication channel in which to propagate call-derived vibrations [2]. Insects on vegetation often use leaves and stems as substrates through which they transmit and receive seismic signals [3]. Here we report that golden rocket frogs calling from their natural substrate generate plant-borne vibrations, and we show that these vibrations can change the frog's behavior. This suggests that plant-borne vibrations can play a role in both modifying the call structure of a vertebrate and directing its movements on the substrate.