The dawn of social bonds: what is the role of shared experiences in non-human animals?

Group-living animals can develop social bonds. Social bonds can be considered a type of social relationship characterized by frequent and consistent affiliative (non-reproductive) interactions. Social bonds with conspecifics bring many advantages, also in terms of direct fitness. A characteristic of social bonds is that they need time to develop. Several studies on humans have emphasized the fact that sharing experiences can affect the strength of social bonds. A similar trend can be spotted in non-human species. For example, a recent experiment showed that if chimpanzees watched a video together with a conspecific, they spent more time in proximity compared to conspecifics with whom they did not actively watch a video. Another experiment on fish showed that individuals who experienced a situation of high predation risk together, showed preference for each other compared to those who did not. As the link between shared experiences and social bonds is not explicitly recognized in non-human animals, the main goal of this work is to propose the exploration of this novel research path. This exploration would contribute to shed light on the evolutionary mechanisms of social bond (or friendship) development and maintenance between individuals in different vertebrate species, from fish to non-human primates.

Information about Predators Varies across an Amazonian Rain Forest as a Result of Sentinel Species Distribution.

Information about predation risk is of fundamental value in biological communities. Because many prey species have shared predators, eavesdropping on other species' alarms is a widely recognized mechanism underlying the formation of mixed-species groups. However, information transfer may vary both across and within groups because some species provide higher-quality information about predators than others. We tested this phenomenon in Amazonian understory mixed-species flocks of birds in which two sentinel species-the bluish-slate antshrike (Thamnomanes schistogynus) and the dusky-throated antshrike (Thamnomanes ardesiacus)-occupy different habitats and provide alarm calls that are used by eavesdropping flock mates. In a playback experiment, two associate species responded significantly more strongly to alarm calls from the same sentinel species, reflecting the greater reliability of information about predator threats that could affect survival and habitat choice. Our work provides evidence of a repeated asymmetry across space in the available information about threats.

Familiarity and sex modulate size-dependent following behaviour in the Mediterranean killifish.

Living in a group offers the chance to follow the choices and the behaviours of other individuals. Following a group mate might confer fitness advantages if the group mate knows about resources such as food or shelters. Shoaling fish often follow larger group mates which, in most species, are generally older and therefore more experienced. Yet, the effect of individuals' characteristics other than size on following behaviour remains to be understood. For example, familiar fish and female shoals have been reported as more cohesive, which might be due to a differential tendency to follow in relation to familiarity and sex. Here, we investigated whether size, familiarity, sex, and the interaction between these factors affect fish following behaviour. We observed pairs of differently sized Mediterranean killifish, Aphanius fasciatus, exploring a new environment, and we recorded whether the rear fish followed the front fish when the latter changed swimming direction. In female and male pairs, and in unfamiliar pairs, smaller fish were more likely to follow the directional change of the larger fish than vice versa. In mixed-sex pairs and in familiar pairs, however, size did not affect following behaviour and larger fish followed as much as smaller fish did. Our results revealed that killifish's following decisions are determined by the size of the individuals, their level of familiarity, and their sex. These characteristics may have a notable impact on the behaviour of fish groups in nature.

House sparrows' (Passer domesticus) behaviour in a novel environment is modulated by social context and familiarity in a sex-specific manner.

BACKGROUND: Exploratory behaviour is one of the best-investigated behavioural traits. However, little is known about how differences in familiarity, i.e. in the knowledge and previous experience with a companion can influence the exploration of a novel environment. However, to our knowledge, such a critical feature of the social environment has never been the target of a study relating it to exploratory behaviour in birds. Here we examined if familiarity with a conspecific could affect behavioural responses of individuals confronted with a novel environment. We recorded the latency to land on the ground, latency to feed, time spent feeding and number of sectors visited of 48 female and 48 male house sparrows (Passer domesticus) in an indoor aviary in three contexts: alone (individual context), with an unfamiliar and with a familiar same-sex companion. RESULTS: House sparrows landed sooner on the ground when in the familiar context than when in the individual context. Birds in unfamiliar pairs followed each other less than familiar birds, but this difference diminished with time spent exploring. Moreover, males and females differed in their behavioural responses in the unfamiliar context. Females with a familiar companion landed sooner than when they were paired with an unfamiliar conspecific, whereas only the presence of a companion but not familiarity reduced males latency to land on the ground. Finally, when considering the unfamiliar context males had shorter latencies to forage and thus spent more time eating than females. CONCLUSIONS: The presence or absence of a companion and its familiarity with the focal individual influenced differently the behavioural responses of male and female house sparrows in a novel environment. As house sparrows are strongly sociable, the influence of the social environment is likely to be of paramount importance to understand the selective pressures acting on them, particularly in recently colonized areas with ephemeral food sources. Our results shed light on the complex influence that the social environment has on the behavioural responses of a cosmopolitan bird.

Within-shoal phenotypic homogeneity affects shoaling preference in a killifish.

Anti-predator benefits associated with living in groups are multiple and taxonomically widespread. In fish shoals, individuals can exploit the confusion effect, whereby predators struggle to target a single individual among several individuals. Theory predicts that the confusion effect could be aided by homogeneity in appearance; thus, individuals should group by phenotypic characteristics, contributing to generating high within-shoal phenotypic homogeneity. While assortments by body size have been extensively documented, almost nothing is known about whether within-shoal homogeneity in body pigmentation affects shoaling preference. To investigate this issue, we used the Mediterranean killifish, Aphanius fasciatus, a shoaling species characterized by conspicuous vertical bars on body sides. Individual females were given a choice between two novel shoals characterized by either a high or low degree of homogeneity in the number of bars. As predicted, individual females preferentially associated with the shoal showing the higher phenotypic homogeneity. Our data demonstrated that fish might associate with the shoal that maximizes phenotypic homogeneity in body pigmentation, irrespective of their own phenotype.

Naive tadpoles do not recognize recent invasive predatory fishes as dangerous.

Invasive alien predators (IAP) are spreading on a global scale-often with devastating ecological effects. One reason for their success may be that prey species fail to recognize them due to a lack of co-evolutionary history. We performed a comprehensive test of this "prey naiveté" hypothesis using a novel approach: we tested whether predator-naive tadpoles of the agile frog (Rana dalmatina) display antipredator behavior upon encountering chemical cues produced by native, invasive (established or recent) or allopatric fishes (four perciforms, four siluriforms, and two cypriniforms). We studied the influence of population origin on predator-detection ability by presenting chemical cues to predator-naive tadpoles that originated from fishless hill-ponds or fish-infested floodplain populations. Before trials, we fed fishes with tadpoles or an alternative food to test whether direct chemical cues from the predator's diet influences the tadpoles' recognition of potential predators. Tadpoles reduced their activity upon exposure to cues from native and long-established invasive perciforms, but not in response to recent invaders, allopatric predators, or to any siluriforms. Also, predators that were previously fed with tadpoles did not universally induce behavioral defensedefenses upon first encounter. Finally, tadpoles originating from isolated hill-ponds exhibited higher baseline activity and responded in weaker fashion than their conspecifics from floodplain populations, which co-exist with predatory fishes. Our results indicate that tadpoles may be vulnerable to invading predatory fishes due to their inability to recognize them as dangerous, though their ability to recognize invasive IAP may evolve rapidly, in fewer than 30 generations.

Reproductive interference between Rana dalmatina and Rana temporaria affects reproductive success in natural populations.

Experimental evidence suggests that reproductive interference between heterospecifics can seriously affect individual fitness; support from field studies for such an effect has, however, remained scarce. We studied reproductive interference in 25 natural breeding ponds in an area where two ranid frogs, Rana dalmatina and Rana temporaria, co-occur. The breeding seasons of the two species usually overlap and males of both species are often found in amplexus with heterospecific females, even though matings between heterospecifics produce no viable offspring. We estimated species abundance ratios based on the number of clutches laid and evaluated fertilization success. In ponds with low spatial complexity and a species abundance ratio biased towards R. temporaria, the average fertilization success of R. dalmatina eggs decreased, while this relationship was not detectable in spatially more complex ponds. Fertilization success of R. temporaria did not decrease with increasing relative numbers of heterospecifics. This asymmetry in fitness effects of reproductive interference may be attributed to R. temporaria males being more competitive in scramble competition for females than R. dalmatina males. Our study is among the first to demonstrate that in natural breeding populations of vertebrates interference among heterospecifics has the potential to substantially lower reproductive success at the population level, which may in turn affect population dynamics.

The great tit HapMap project: A continental-scale analysis of genomic variation in a songbird.

A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude - almost the entire geographical range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugium, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear 'islands of differentiation', even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (FST), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species' range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics.

Host response to cuckoo song is predicted by the future risk of brood parasitism.

INTRODUCTION: Risk assessment occurs over different temporal and spatial scales and is selected for when individuals show an adaptive response to a threat. Here, we test if birds respond to the threat of brood parasitism using the acoustical cues of brood parasites in the absence of visual stimuli. We broadcast the playback of song of three brood parasites (Chalcites cuckoo species) and a sympatric non-parasite (striated thornbill, Acanthiza lineata) in the territories of superb fairy-wrens (Malurus cyaneus) during the peak breeding period and opportunistic breeding period. The three cuckoo species differ in brood parasite prevalence and the probability of detection by the host, which we used to rank the risk of parasitism (high risk, moderate risk, low risk). RESULTS: Host birds showed the strongest response to the threat of cuckoo parasitism in accordance with the risk of parasitism. Resident wrens had many alarm calls and close and rapid approach to the playback speaker that was broadcasting song of the high risk brood parasite (Horsfield's bronze-cuckoo, C. basalis) across the year (peak and opportunistic breeding period), some response to the moderate risk brood parasite (shining bronze-cuckoo, C. lucidus) during the peak breeding period, and the weakest response to the low risk brood parasite (little bronze-cuckoo, C. minutillus). Playback of the familiar control stimulus in wren territories evoked the least response. CONCLUSION: Host response to the threat of cuckoo parasitism was assessed using vocal cues of the cuckoo and was predicted by the risk of future parasitism.

Mate choice is affected by parasite infestation rate of the choosing individual as well as of potential mating partners.

Parasites are known to be a key driving force in mate choice and are important for the expression and evolution of ornaments and behavioral traits being used. However, there is little experimental evidence on how the parasite's burden of the choosing individual is integrated into the mate-choice process and how it affects decision-making, especially in relation to parasite infestation of potential mates. Thus, the aim of our study was to determine whether female house sparrows Passer domesticus adjust their mate preference according to their own as well as the parasite load of prospective partners. To do this, we experimentally manipulated female parasite load and determined their mate preferences prior to and after parasite treatment. We manipulated the chronic coccidian parasite burden of females either by initiating the acute infection phase via re-infecting them with coccidian or by temporally reducing the parasite load of coccidia. We then measured the effect of this manipulation on mate preference by presenting females with a choice of four stimuli: three males with similar ornaments, but unmanipulated, naturally varying chronic coccidiosis levels, and an unmanipulated control female. Additionally, we recorded some males' behavior in relation to their infection status pointing toward an increased or reduced interest in mating. We found that females preferred highly infested males prior to manipulation, regardless of their own infestation level. However, after manipulation, infested females avoided highly infested males probably in response to the deterioration of their health condition by parasites. Our study suggests that mate-choice decisions are more complex when they are mediated by parasites. The implications of parasites for evolutionary theories of sexual signaling and mate choice are discussed.

Female attractiveness affects paternal investment: experimental evidence for male differential allocation in blue tits.

INTRODUCTION: The differential allocation hypothesis (DAH) predicts that individuals should adjust their parental investment to their current mate's quality. Although in principle the DAH holds for both sexes, male adjustment of parental investment has only been tested in a few experimental studies, revealing contradictory results. We conducted a field experiment to test whether male blue tits (Cyanistes caeruleus) allocate their parental effort in relation to female ornamentation (ultraviolet colouration of the crown), as predicted by the DAH. RESULTS: We reduced the UV reflectance in a sample of females and compared parental care by their mates with that of males paired to sham-manipulated control females. As predicted by the DAH our results demonstrate that males paired with UV-reduced females invested less in feeding effort but did not defend the chicks less than males paired with control females. CONCLUSIONS: To our knowledge, this is one of the first studies providing support for male differential allocation in response to female ornamentation.

Female house sparrows "count on" male genes: experimental evidence for MHC-dependent mate preference in birds.

BACKGROUND: Females can potentially assess the quality of potential mates using their secondary sexual traits, and obtain "good genes" that increase offspring fitness. Another potential indirect benefit from mating preferences is genetic compatibility, which does not require extravagant or viability indicator traits. Several studies with mammals and fish indicate that the genes of the major histocompatibility complex (MHC) influence olfactory cues and mating preferences, and such preferences confer genetic benefits to offspring. We investigated whether individual MHC diversity (class I) influences mating preferences in house sparrows (Passer domesticus). RESULTS: Overall, we found no evidence that females preferred males with high individual MHC diversity. Yet, when we considered individual MHC allelic diversity of the females, we found that females with a low number of alleles were most attracted to males carrying a high number of MHC alleles, which might reflect a mating-up preference by allele counting. CONCLUSIONS: This is the first experimental evidence for MHC-dependent mating preferences in an avian species to our knowledge. Our findings raise questions about the underlying mechanisms through which birds discriminate individual MHC diversity among conspecifics, and they suggest a novel mechanism through which mating preferences might promote the evolution of MHC polymorphisms and generate positive selection for duplicated MHC loci.

Only females in poor condition display a clear preference and prefer males with an average badge.

BACKGROUND: Female condition-dependent variation in mate preference may have important evolutionary implications, not only within the same population but also among populations. There are few experiments, however, on how condition and/or genotype influences female mate preferences. The black throat patch of the male house sparrow, Passer domesticus, is an intensively studied plumage trait. It is often referred to as a 'badge of status' and seems to be involved in female mate choice, but differences exist among populations. Between-population variation in mate preference may occur for condition-dependent mate preferences. We tested the hypothesis that female preference may vary with female quality (body condition). Therefore, we measured female preference for badge size using an aviary two-choice test in which females were presented with two males that had different sizes of badges (enlarged or averaged). RESULTS: Overall we did not find a female preference for enlarged or average badges, but low-quality females spent more time near average badge males. Conversely, high-quality females did not show a clear preference. CONCLUSIONS: Collectively, these results indicate that female preference varies with female quality. Differences in female condition are causes of within-population variation in mating preferences. To our knowledge, our results provide one of the first experimental evidences that variation in preference for a male ornament is associated with female condition. In our study, however, only females of low condition displayed a clear mate preference. Differences observed among populations could be partly explained by differences in female condition.

Flock-dependent exploitation of a limited resource in House Sparrow.

The performances of different social groups can depend on various characteristics, such as familiarity among their members or the presence of individuals with specific traits. However, it has rarely been investigated how groups perform during an encounter with other conspecifics, even if in the natural environment social groups often run into each other and compete for resources. We investigated whether a certain characteristic of the group (i.e., familiarity) could benefit its members when they are confronted with another group. We designed a novel experimental set-up, creating triads of captive house sparrows (Passer domesticus) and examining whether in a situation of competition for limited resources one triad could gain benefits over the other (consume more mealworms, Tenebrio molitor). While we did not find an effect of previous familiarity among triad members on the triads' performances, we discovered a group-based difference in the number of mealworms eaten per capita. Group-mates of the very first individual to eat a mealworm (first feeder) ate more mealworms than those in the opposing triad. First feeder individuals also foraged sooner and more than other birds in a subsequent prey consumption assay. Our results suggest that individual performances were influenced by group membership, even when groups were exploiting the same resource simultaneously.

Inter-individual differences in foraging tactics of a colonial raptor: consistency, weather effects, and fitness correlates.

BACKGROUND: Consistent inter-individual differences in behavioural phenotypes may entail differences in energy efficiency and expenditure, with different fitness payoffs. In colonial-breeding species, inter-individual differences in foraging behaviour may evolve to reduce resource use overlap among conspecifics exploiting shared foraging areas. Furthermore, individual differences in foraging behaviour may covary with individual characteristics, such as sex or physiological conditions. METHODS: We investigated individual differences in foraging tactics of a colonial raptor, the lesser kestrel (Falco naumanni). We tracked foraging trips of breeding individuals using miniaturized biologgers. We classified behaviours from GPS data and identified tactics at the foraging trip level by cluster analysis. We then estimated energy expenditure associated to each tactic from tri-axial accelerometer data. RESULTS: We obtained 489 foraging trips by 36 individuals. Two clusters of trips were identified, one (SF) characterized by more static foraging behaviour and the other (DF) by more dynamic foraging behaviour, with a higher proportion of flying activity and a higher energy expenditure compared to SF. Lesser kestrels showed consistent inter-individual differences in foraging tactics across weather condition gradients, favouring DF trips as solar radiation and crosswind intensity increased. DF trips were more frequent during the nestling-rearing than during the egg incubation stage. Nestlings whose tracked parent was more prone to perform DF trips experienced higher daily mass increase, irrespective of nestling feeding rates. CONCLUSIONS: Our study provided evidence that breeding lesser kestrels flexibly adopted different foraging tactics according to contingent weather landscapes, with birds showing consistent inter-individual differences in the tendency to adopt a given tactic. The positive correlation between the tendency to perform more energy-demanding DF trips and nestling growth suggests that individual differences in foraging behaviour may play a role in maintaining key life-history trade-offs between reproduction and self-maintenance.

Can house sparrows recognize familiar or kin-related individuals by scent?

In the last decades, higher attention has been paid to olfactory perception in birds. As a consequence, a handful of avian species have been discovered to use olfaction in different contexts. Nevertheless, we still have a very limited knowledge about the use of odor cues in avian social life, particularly, in the case of songbirds. Here, we investigate if female house sparrows Passer domesticus show any preference for the odor of kin and nonkin conspecifics and we also test a possible role of familiarity based on male scent in female choice. We performed the experiment with captive birds twice, during the nonbreeding and breeding seasons. Our results show that female house sparrows strongly avoided the odor of unrelated familiar (UF) males, both in the breeding and nonbreeding seasons. Our results suggest recognition for olfactory stimuli related to familiarity and kinship. We suggest that avoidance for UF males is associated with previous experience in this species. Also, we provided further evidence to the use of olfaction in passerine species by using a new experimental setup.

Spatial segregation of home ranges between neighbouring colonies in a diurnal raptor.

Enhancement of information transfer has been proposed as a key driver of the evolution of coloniality. Transfer of information on location of food resources implies that individuals from the same colony share foraging areas and that each colony can be associated to a specific foraging area. In colonial breeding vertebrates, colony-specific foraging areas are often spatially segregated, mitigating intercolony intraspecific competition. By means of simultaneous GPS tracking of lesser kestrels (Falco naumanni) from neighbouring colonies, we showed a clear segregation of space use between individuals from different colonies. Foraging birds from different neighbouring colonies had home ranges that were significantly more segregated in space than expected by chance. This was the case both between large and between small neighbouring colonies. To our knowledge, the lesser kestrel is the only terrestrial species where evidence of spatial segregation of home ranges between conspecifics from neighbouring colonies has been demonstrated. The observed spatial segregation pattern is consistent with the occurrence of public information transfer about foraging areas and with the avoidance of overexploited areas located between neighbouring colonies. Our findings support the idea that spatial segregation of exploited areas may be widespread among colonial avian taxa, irrespective of colony size.

Home, dirty home: effect of old nest material on nest-site selection and breeding performance in a cavity-nesting raptor.

The quality of a breeding site may have major fitness consequences. A fundamental step to understanding the process of nest-site selection is the identification of the information individuals use to choose high-quality nest sites. For secondary cavity-nesting bird species that do not add nest lining material, organic remains (faeces, pellets) accumulated inside nest cavities during previous breeding events may be a cue for high-quality nest-sites, as they contain information about past successful breeding and may improve thermal insulation of eggs during incubation. However, cavities in which breeding was successful might also contain more nest-dwelling ectoparasites than unoccupied cavities, offering an incentive for prospective parents to avoid them. We exposed breeding cavity-nesting lesser kestrels (Falco naumanni) to nestbox dyads consisting of a dirty (with a thick layer of organic substrate) and a clean nestbox (without organic material). Dirty nestboxes were strongly preferred, being occupied earlier and more frequently than clean ones. Hatching success in dirty nestboxes was significantly higher than in clean ones, suggesting a positive effect of organic nest material on incubation efficiency, while nestbox dirtiness did not significantly affect clutch and brood size. Nestlings from dirty nestboxes had significantly higher ectoparasite load than those from clean nestboxes soon after egg hatching, but this difference was not evident a few days later. Nest substrate did not significantly affect nestling growth. We concluded that nest substrate is a key driver of nest-site choice in lesser kestrels, although the adaptive value of such a strong preference appears elusive and may be context-dependent.

Sex composition modulates the effects of familiarity in new environment.

In many social species, when an individual is associated with familiar conspecifics, it displays an array of behaviours that may confer benefits (e.g., increased boldness and faster habituation to novel environments). In fish, these effects of familiarity have been studied using individuals of only one sex or juveniles. Since shoals often vary regarding sex composition and males and females show different social behaviours, we hypothesised that social familiarity's effects vary with group sex composition. We tested this hypothesis by comparing the exploratory behaviour of groups of two females, two males, and one male and one female Mediterranean killifish, Aphanius fasciatus, which were either familiar or unfamiliar. Pairs of familiar females were bolder than pairs of unfamiliar females, whereas males showed the opposite trend. Pairs of familiar females also showed faster habituation to the novel environment and, at the beginning of the test, were more cohesive compared to pairs of unfamiliar females. Pairs of familiar mixed-sex fish habituated faster to the novel environment than unfamiliar pairs. Pairs of familiar males did not show any beneficial effect of familiarity relative to pairs of unfamiliar males. Hence, the effects of social familiarity on exploratory behaviour, and likely the associated benefits, appear to depend on the sex composition of the pair in the Mediterranean killifish.

Eggshell coloration and its importance in postmating sexual selection.

Avian eggshell color seems to fulfill multiple functions, some of them being structural and others signaling. In this study, we tested whether or not eggshell coloration may play a role in sexual selection of Tree Sparrows (Passer montanus). According to the "Sexually selected eggshell coloration" hypothesis, eggshell coloration signals female, egg or chick quality and males adjust parental investment according to this signal. Eggs of this species are covered with brown spots and patches, and variation between clutches is high. We found that eggshell coloration correlates with both protoporphyrin and biliverdin, but protoporphyrin concentrations are ten times higher. Eggshell coloration reflects egg and offspring quality, but not female quality. Thus, eggshell coloration may signal female postmating investment in offspring rather than female quality. Furthermore, differential allocation in terms of maternal investment is supported by the fact that females lay more pigmented clutches when mated to males with bigger melanin-based ornaments relative to their own. Moreover, males invested proportionally more to chicks that hatched from more pigmented clutches. Our correlative results thus seem to support a role of sexual selection in the evolution of eggshell coloration in birds laying brown eggs, pigmented mainly by protoporphyrin.