Experimental evidence that chronic outgroup conflict reduces reproductive success in a cooperatively breeding fish

Conflicts with conspecific outsiders are common in group-living species, from ants to primates, and are argued to be an important selective force in social evolution. However, whilst an extensive empirical literature exists on the behaviour exhibited during and immediately after interactions with rivals, only very few observational studies have considered the cumulative fitness consequences of outgroup conflict. Using a cooperatively breeding fish, the daffodil cichlid (Neolamprologus pulcher), we conducted the first experimental test of the effects of chronic outgroup conflict on reproductive investment and output. ‘Intruded’ groups received long-term simulated territorial intrusions by neighbours that generated consistent group-defence behaviour; matched ‘Control’ groups (each the same size and with the same neighbours as an Intruded group) received no intrusions in the same period. Intruded groups had longer inter-clutch intervals and produced eggs with increasingly less protein than Control groups. Despite the lower egg investment, Intruded groups provided more parental care and achieved similar hatching success to Control groups. Ultimately, however, Intruded groups had fewer and smaller surviving offspring than Control groups at 1-month post-hatching. We therefore provide experimental evidence that outgroup conflict can decrease fitness via cumulative effects on reproductive success, confirming the selective potential of this empirically neglected aspect of sociality

Fitness consequences of outgroup conflict

In social species across the animal kingdom, conspecific outsiders threaten the valuable resources of groups and their members. This outgroup conflict is recognised as a powerful selection pressure, but we argue that studies explicitly quantifying the fitness consequences need to be broader in scope: more attention should be paid to delayed, cumulative, and third-party fitness consequences, not just those arising immediately to group members involved in physical contests. In the first part of this review, we begin by documenting how single contests can have survival and reproductive consequences either immediately or with a delay. Then, we step beyond contests to describe fitness consequences that can also result from interactions with cues of rival presence and the general landscape of outgroup threat, and beyond single interactions to describe cumulative effects of territorial pressure and elevated outgroup-induced stress. Using examples from a range of taxa, we discuss which individuals are affected negatively and positively, considering both interaction participants and third-party group members of the same or the next generation. In the second part of the review, we provide suggestions about how to move forward. We highlight the importance of considering how different types of outgroup conflict can generate different selection pressures and of investigating variation in fitness consequences within and between species. We finish by discussing the value of theoretical modelling and long-term studies of natural populations, experimental manipulations, and meta-analyses to develop further our understanding of this crucial aspect of sociality

Variation between species, populations, groups and individuals in the fitness consequences of outgroup conflict

Out-group conflict is rife in the natural world, occurring from primates to ants. Traditionally, research on this aspect of sociality has focused on the interactions between groups and their conspecific rivals, investigating contest function and characteristics, which group members participate and what determines who wins. In recent years, however, there has been increasing interest in the consequences of out-group conflict. In this review, we first set the scene by outlining the fitness consequences that can arise immediately to contest participants, as well as a broader range of delayed, cumulative and third-party effects of out-group conflict on survival and reproductive success. For the majority of the review, we then focus on variation in these fitness consequences of out-group conflict, describing known examples both between species and between populations, groups and individuals of the same species. Throughout, we suggest possible reasons for the variation, provide examples from a diverse array of taxa, and suggest what is needed to advance this burgeoning area of social evolution. This article is part of the theme issue ‘Intergroup conflict across taxa’

Impacts of additional noise on the social interactions of a cooperatively breeding fish

Anthropogenic noise is a global pollutant known to affect the behaviour of individual animals in all taxa studied. However, there has been relatively little experimental testing of the effects of additional noise on social interactions between conspecifics, despite these forming a crucial aspect of daily life for most species. Here we use established paradigms to investigate how white-noise playback affects both group defensive actions against an intruder and associated within-group behaviours in a model fish species, the cooperatively breeding cichlid Neolamprologus pulcher. Additional noise did not alter defensive behaviour, but did result in changes to within-group behaviour. Both dominant and subordinate females, but not the dominant male, exhibited less affiliation and showed a tendency to produce more submissive displays to groupmates when there was additional noise compared to control conditions. Our experimental results therefore indicate the potential for anthropogenic noise to affect social interactions between conspecifics and that there can be intraspecific variation in the impacts of this global pollutant.Spreadsheet of study results includes four excel tabs, corresponding to each of the main elements of the manuscript: defensive actions against intruders, within-group affiliation displayed, within-group aggression displayed, and within-group submission displayed. DF = dominant female, DM = dominant male, S = subordinate. Funding provided by: European Research CouncilCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100000781Award Number: 682253To investigate the influence of additional noise on territory defence and associated within-group behaviour, we gave 16 groups of daffodil cichlids (Neolamprologus pulcher) two treatments each in a repeated-measures design: during the simulated territorial intrusion of a rival female, there was playback of either white noise (additional noise) or silence (loudspeaker turned on but not playing any sound, as a control). We video-recorded all trials and scored behaviours using the ethogram from Braga Goncalves et al,. 2020. For each 10-min intrusion period, we scored defensive behaviours for each category of individual (DM, DF, SF) and the total amount received by the intruder. We also scored all affiliation and aggression displayed to other group members by each category of individual during the intrusion period. We examined the effect of additional noise on the total defensive effort against the intruder; we then determined whether the non-significant treatment difference was consistent across all three individual categories or if there were counterbalancing effects between group members. Second, we investigated the effect of additional noise on the overall amount of within-group aggression, affiliation and submission exhibited; we used the sequential Bonferroni correction as there was a separate test for each behaviour. For those behaviours found to be significantly different between treatments (affiliation and submission; see Results), we determined which group members were driving the differences

Phylogeography of the snake pipefish, <i>Entelurus aequoreus</i> (Family: Syngnathidae) in the northeastern Atlantic Ocean

The snake pipefish, Entelurus aequoreus, is a widespread marine species occurring in pelagic and coastal environments in the northeastern Atlantic Ocean. Recently, the snake pipefish underwent a short-lived, yet substantial, increase in abundance and range expansion into arctic waters. However, little is known about the species' population structure or if different ecotypes contributed to this outbreak. Specimens (n = 178) were sampled from 25 locations from six regions spanning 1.9 million km2. A fragment of the mitochondrial cytochrome b gene and control region was used to assess population structure and genetic diversity. Both loci showed high haplotype diversity (Hd) and low nucleotide diversity (π) over all sampled locations. A genetic signature of population expansion was evident through mismatch distributions and tests for recent population expansion (Fu's Fs, Tajima's D and R2). Effective population size analyses (Bayesian skyline plot) suggest an expansion 50-100 thousand years before present. However, we found neither significant population differentiation (analysis of molecular variance) among regions nor evidence of genetically distinct ecotypes. This lack of structure is probably due to a pelagic life style, fast development and long distance dispersal aided by ocean currents. Our work highlights the need for further research to better understand the recent outbreak and how this species may respond to future environmental challenge

Validation of a fecal glucocorticoid assay to assess adrenocortical activity in meerkats using physiological and biological stimuli

In mammals, glucocorticoid (i.e. GC) levels have been associated with specific life-history stages and transitions, reproductive strategies, and a plethora of behaviors. Assessment of adrenocortical activity via measurement of glucocorticoid metabolites in feces (FGCM) has greatly facilitated data collection from wild animals, due to its non-invasive nature, and thus has become an established tool in behavioral ecology and conservation biology. The aim of our study was to validate a fecal glucocorticoid assay for assessing adrenocortical activity in meerkats (Suricata suricatta), by comparing the suitability of three GC enzyme immunoassays (corticosterone, 11β-hydroxyetiocholanolone and 11oxo-etiocholanolone) in detecting FGCM increases in adult males and females following a pharmacological challenge with adrenocorticotropic hormone (ACTH) and biological stimuli. In addition, we investigated the time course characterizing FGCM excretion, the effect of age, sex and time of day on FGCM levels and assessed the potential effects of soil contamination (sand) on FGCM patterns. Our results show that the group specific 11β-hydroxyetiocholanolone assay was most sensitive to FGCM alterations, detecting significant and most distinctive elevations in FGCM levels around 25 h after ACTH administration. We found no age and sex differences in basal FGCM or on peak response levels to ACTH, but a marked diurnal pattern, with FGCM levels being substantially higher in the morning than later during the day. Soil contamination did not significantly affect FGCM patterns. Our results emphasize the importance of conducting assay validations to characterize species-specific endocrine excretion patterns, a crucial step to all animal endocrinology studies using a non-invasive approach.SUPPORTING INFORMATION : S1 FILE. Group FGCM response (median ± SE, μg/g) to a natural attack on a group member (ZIM005) that resulted in its permanent eviction. The victim showed the greatest FGCM response to the event. Group FGCM levels returned to baseline levels after the male was removed from the colony. “Within 48 h” represent FGCM levels measured within 2 days after the attack on M5 took place. = p < 0.01 (Fig A). Average (median ± SE) baseline FGCM levels (μg/g) in fecal samples deposited in the morning (AM), at midday (MD) and late afternoon (PM), as measured with the 11β-hydroxyetiocholanolone assay. N = 128 fecal samples from 13 individuals. = p < 0.05 (Fig B). Remove selectedThe Swiss National Science Foundation (grant no. 31003A_13676) to Marta B. Manser, the University of Zurich, and by an ERC grant (no. 294494, THCB2011) to Tim H. Clutton-Brock at the University of Cambridge.http://www.plosone.orgam2016Anatomy and Physiolog

The influence of stress hormones and aggression on cooperative behaviour in subordinate meerkats

In cooperative breeders, aggression from dominant breeders directed at subordinates may raise subordinate stress hormone (glucocorticoid) concentrations. This may benefit dominants by suppressing subordinate reproduction but it is uncertain whether aggression from dominants can elevate subordinate cooperative behaviour, or how resulting changes in subordinate glucocorticoid concentrations affect their cooperative behaviour. We show here that the effects of manipulating glucocorticoid concentrations in wild meerkats (Suricata suricatta) on cooperative behaviour varied between cooperative activities as well as between the sexes. Subordinates of both sexes treated with a glucocorticoid receptor antagonist (mifepristone) exhibited significantly more pup protection behaviour (babysitting) compared to those treated with glucocorticoids (cortisol) or controls. Females treated with mifepristone had a higher probability of exhibiting pup food provisioning (pup-feeding) compared to those treated with cortisol. In males, there were no treatment effects on the probability of pup-feeding, but those treated with cortisol gave a higher proportion of the food they found to pups than those treated with mifepristone. Using 19 years of behavioural data, we also show that dominant females did not increase the frequency with which they directed aggression at subordinates at times when the need for assistance was highest. Our results suggest that it is unlikely that dominant females manipulate the cooperative behaviour of subordinates through the effects of aggression on their glucocorticoid levels and that the function of aggression directed at subordinates is probably to reduce the probability they will breed

Exorcising Grice’s ghost : an empirical approach to studying intentional communication in animals

Language’s intentional nature has been highlighted as a crucial feature distinguishing it from other communication systems. Specifically, language is often thought to depend on highly structured intentional action and mutual mindreading by a communicator and recipient. Whilst similar abilities in animals can shed light on the evolution of intentionality, they remain challenging to detect unambiguously. We revisit animal intentional communication and suggest that progress in identifying analogous capacities has been complicated by (i) the assumption that intentional (that is, voluntary) production of communicative acts requires mental-state attribution, and (ii) variation in approaches investigating communication across sensory modalities. To move forward, we argue that a framework fusing research across modalities and species is required. We structure intentional communication into a series of requirements, each of which can be operationalised, investigated empirically, and must be met for purposive, intentionally communicative acts to be demonstrated. Our unified approach helps elucidate the distribution of animal intentional communication and subsequently serves to clarify what is meant by attributions of intentional communication in animals and humans

Beyond aggression: Androgen-receptor blockade modulates social interaction in wild meerkats

In male vertebrates, androgens are inextricably linked to reproduction, social dominance, and aggression, often at the cost of paternal investment or prosociality. Testosterone is invoked to explain rank-related reproductive differences, but its role within a status class, particularly among subordinates, is underappreciated. Recent evidence, especially for monogamous and cooperatively breeding species, suggests broader androgenic mediation of adult social interaction. We explored the actions of androgens in subordinate, male members of a cooperatively breeding species, the meerkat (Suricata suricatta). Although male meerkats show no rank-related testosterone differences, subordinate helpers rarely reproduce. We blocked androgen receptors, in the field, by treating subordinate males with the antiandrogen, flutamide. We monitored androgen concentrations (via baseline serum and time-sequential fecal sampling) and recorded behavior within their groups (via focal observation). Relative to controls, flutamide-treated animals initiated less and received more high-intensity aggression (biting, threatening, feeding competition), engaged in more prosocial behavior (social sniffing, grooming, huddling), and less frequently initiated play or assumed a ‘dominant’ role during play, revealing significant androgenic effects across a broad range of social behavior. By contrast, guarding or vigilance and measures of olfactory and vocal communication in subordinate males appeared unaffected by flutamide treatment. Thus, androgens in male meerkat helpers are aligned with the traditional trade-off between promoting reproductive and aggressive behavior at a cost to affiliation. Our findings, based on rare endocrine manipulation in wild mammals, show a more pervasive role for androgens in adult social behavior than is often recognized, with possible relevance for understanding tradeoffs in cooperative systems