Ecology

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Funicular bodies: structure, function, and developmentThe ultrastructural and functional complexity of funicular bodies in bryozoans25,46,47 (our data), as well as the reduction of the genome in their symbiotic bacteria (e.g., Bugula neritina48), point at a long-term co-evolution between these organisms, also suggesting that infected bryozoan colonies spend a significant part of their energy budget supporting numerous bacteria inside FBs. All known prokaryote symbionts are apparently non-pathogenic for bryozoans49,62. Instead, the overall evidence indicates a mutualistic relationship. Symbiotic bacteria are known to produce toxic substances (bryostatins in Bugula63; bryoanthrathiophene in Watersipora64) that protect bryozoan larvae from predators42,44,45. Another potential role of bacterial secondary metabolites is the chemical defense of early developmental stages during larval settlement and metamorphosis40,65. Such chemical defence may also prevent epibiotic overgrowth of the bryozoan colonies by other bacteria and algae (reviewed in66,67). Similar functions can be assumed for symbiotic prokaryotes of Dendrobeania fruticosa, although experimental evidence is still required.FBs with bacterial symbionts in colonies of D. fruticosa show signs of high specialization. The walls of the funicular body completely isolate its internal cavity from the surrounding zooidal cavity: the cells of the outer layer overlap each other, whereas cells of the inner layer have tight Z-shaped contacts. Such isolation probably creates a specific environment inside the symbiont-containing space that helps maintain a growing population of bacterial symbionts. A massive protein-synthesizing apparatus was observed in the cells of the inner layer. In addition, the ‘pocket’-like structure of the internal cavity of FB and the abundance of cytoplasmic processes, some of which protruded deep into this cavity, contribute to increasing both the general inner surface area of FB and the contact area between its inner cells and bacteria. From their side, bacteria provide this contact by numerous pili. Numerous pits and microvesicles associated with the apical membrane of the inner cells imply an active exchange of substances between the host and its symbionts (e.g., nutrition provided to growing and multiplying bacteria and absorption of the potential wastes they produce).The ultrastructure and functional morphology of FBs in Aquiloniella scabra, the only species in which the ultrastructure of these organs was described, are very similar to those in D. fruticosa. Its FBs also consist of two cell types, but the inner cell layer is formed by one or a few cells, whereas external cells form a multilayered envelope25. In both species, the main function of FBs was considered to be the chambers/organs for symbiont incubation and nourishment.FBs with symbiotic bacteria have been found in several bryozoan species from four different families20,25,47,49,51 (our data). Remarkably, all these families (Bugulidae, Beaniidae, Candidae, Epistomiidae) belong to the clade Buguloidea. Encapsulated aggregations of bacteria within the zooidal cavity were also described in two species of Watersipora from the phylogenetically distant family Watersiporidae (Smittinoidea)62,68. In that case, prokaryotes (“mollicutes”) were also enveloped by flattened bryozoan cells, although the current scarcity of data makes it difficult to compare these cell aggregations with funicular bodies.Among Buguloidea, FBs show the same basic structure, although species described by Lutaud49, Dyrynda and King51, and Mathew with co-authors46 based on light microscopy require re-examination by TEM. Moreover, FBs are in all instances associated with the funicular system of the colony. This similarity could indicate the single origin of the bacterial symbiosis and FBs within Buguloidea. Still, it remains unknown (although rather probable) whether that system transports nutrients from feeding polypides to FBs because no communication between the lacunae of the funicular cords and the FB internal cavity was detected. Another, more likely option, however, is the independent acquisition of bacteria (see also below) and a similar ‘reaction’ of host tissues to invaders, resulting in the formation of bacterial organs (FB) with a similar bauplan. The presence of incapsulated bacteria in non-related Watersipora supports the second interpretation. Answering this question will require both ultrastructural studies and molecular identification of bacteria.As for the initial source of somatic cells and development of FBs, two variants have been suggested. Describing the development of FBs in Bugulina turbinata, Lutaud49 stated that the epithelial cells of the cystid wall were transformed into the inner cell layer of the FB, whereas peritoneal cells formed its external lining. By contrast, while studying Aquiloniella scabra, Karagodina with co-authors25 suggested that bacteria are engulfed by one of the funicular cells, which becomes a ‘bacteriocyte’ that is later enveloped by neighboring funicular cells. In the latter case, FBs are considered to be modified expanded parts of the funicular system. This is consistent with experiments by Sharp and co-authors40, who detected groups of labeled bacteria in the funicular cords of Bugula neritina, and also multiple bacteria developing inside enlarged funicular cords (in fact, very large FBs) in the related Paralicornia sinuosa20.Our TEM study of FBs in D. fruticosa showed that they are not swollen parts of the funicular cords, as was stated by Vishnyakov with co-authors for B. neritina20. It is more likely that the funicular cords and processes of their cells contact the external cell layer of FBs. According to the third scenario that we present here, the inner cell layer of FBs in D. fruticosa, as well as in other studied bugulids, most likely originates from the coelomocytes which accumulate bacteria via phagocytosis. Such solitary cells were described inside the zooidal cavity in B. neritina20. Instead of being digested, engulfed bacteria could trigger the coelomocyte divisions resulting in the formation of the inner cell layer. In contrast, in A. scabra, the coelomocyte can remain single or undergo only a few divisions. We propose that the external cell layer of FB in D. fruticosa originates from the funicular cells because these cell types are ultrastructurally similar. Finally, it is also possible that the exact process and sources of FB formation differ in different species.Multiple and lobed FBs found in two zooids of D. fruticosa could indicate a potential mode of their multiplication. The case of P. sinuosa requires additional study, but currently we believe that its bacteria-bearing ‘funicular cords’ are very large, elongated FBs, as well (see20).Symbiont circulation in the bryozoan life cycleThe taxonomic diversity of bryozoan hosts and their symbiotic bacteria—supported by a variety of sites in the bryozoan zooids and larvae where symbionts have been found—unambiguously point to multiple independent origins of symbiotic associations between bacteria and cheilostome Bryozoa20,25.Rod-shaped bacteria are the most common symbionts in the superfamily Buguloidea. Although superficially similar, these bacteria strongly differ in their maximum size, suggesting the presence of different procaryote species. Thus, bacteria detected in the larvae of Bugulina simplex and in FBs of Aquiloniella scabra can reach 10 μm in length25,69, while healthy symbionts (see below) inside coelomocytes and presumably peritoneal cells of Bugula neritina were only 2.5 μm long20. The maximum length of bacteria in FBs of D. fruticosa never exceeded 5 μm. Coccoid bacteria in the tentacles of B. neritina were 0.5–0.7 μm in diameter20. Else, oval or irregularly-shaped mycoplasma-like α-Proteobacteria were detected in the genus Watersipora62,68,70. By contrast, the symbionts identified in B. neritina and B. simplex belong to γ-Proteobacteria69,71,72.Apart from FBs, prokaryote symbionts were described extracellularly in colonies of different cheilostome species: in vestibular glands of autozooids, inside polymorphic zooids (avicularia)38,39,50, in tentacles and funicular cords20. They have also been found intracellularly: inside coelomocytes, epithelial and peritoneal cells of the body wall, and pharyngeal cells20,50. In addition, Woollacott and Zimmer73 described bacteria in the ‘channels’ of the funicular cords associated with brood chambers. However, the TEM image they published shows bacteria inside large vacuoles of the funicular cells—seemingly not in the lacunae between these cells, recalling the aforementioned idea of a ‘bacteriocyte’. Finally, bacteria have also been found in the pallial sinus of bryozoan larvae (62,68,74; reviewed in72). All these diverse data have led to two opposite views on the acquisition and circulation of symbionts in the bryozoan life cycle.Discovery of bacteria in both colonies and larvae of B. neritina was regarded as possible evidence of their transmission from larvae to adults74. This assumption was experimentally proven using both labeled bacteria and their metabolites (bryostatins) in the larvae and preancestrulae developing from them40. Moreover, the presence of bacteria within brood chambers (ovicells) in this species was considered as proof for the next step—the transition of symbionts from the colony to the incubated larvae, i.e., the vertical transfer of symbionts. Symbiotic bacteria populating larvae (and making them unpalatable for predators) are incorporated into the preancestrular tissues during larval metamorphosis, and then found inside zooidal buds in early colonies (a symbiont association with the host cells was not specified) and funicular cords of rhizoids in adult colonies40.The next step of the bacterial development could be the formation of FBs as a locus of symbiont reproduction. Mature FBs, full of bacteria, were considered to be the starting point for the transfer of prokaryotes (by an unknown mechanism) from the zooid to the brood cavity (via funicular cords associated with both FB and ovicells), and then to the incubated larvae47. Light microscopic data demonstrated: (1) the association of FBs with tube-like funicular cords47, and (2) the presence of groups of ‘bacterial bodies’ (small aggregations of bacteria) inside the ooecial vesicle (membranous-epithelial ‘plug’ that closes the entrance to the ovicell; mentioned in B. neritina47, and shown in images of the related Bugulina flabellata75,76,77). In addition, ultrastructural data proved the presence of bacteria inside funicular cords, more precisely—inside their funicular cells (see above), “extending to the ooecial vesicle” (73, p. 362). Elsewhere, Sharp and co-authors (40, p. 697) used fluorescence microscopy to demonstrate the presence of bacteria “within the ovicells”, and suggested that they are transported there across the colony via funicular cords that also house bacteria. Combined, all these data imply that bacteria move from FBs to the ooecial vesicle, accumulate there, and then somehow enter the brood cavity, which contains a larva, either through or in-between the epithelial cells and the cuticle of the ooecial vesicle. Findings of bacteria inside larvae and adult colonies of two species from the non-related genus Watersipora62,68 further strengthened the hypothesis of vertical transfer, which has subsequently been widely accepted by many authors20,30,47,78. Despite extensive TEM studies, no bacteria have been found inside the funicular cords in B. neritina (Vishnyakov & Ostrovsky, unpublished data), which contradicts the data of Sharp and coauthors40 obtained by fluorescent microscopy. Accordingly, it was suggested that coelomocytes carry symbionts to the ooecial vesicle instead20.Nonetheless, the hypothesis of vertical transfer faces serious objections based on life history, molecular and morphological data. In Dendrobeania fruticosa in the White Sea, for example, larval production occurs predominantly in autumn (mainly in the distal parts of branches, Fig. 1A), and no bacteria are present in colonies during this period. In addition, molecular population studies revealed that B. neritina is a complex of sibling species, both symbiotic and aposymbiotic, some of which live in sympatry, with the horizontal transfer between colonies being the most parsimonious explanation for the distribution of bacteria between siblings79. A study of the genome of symbiotic bacteria showed that they may be able to live outside the host48, which is consistent with the hypothesis of horizontal transfer (which is not the same as environmental transmission, see below).TEM data showed no communication between the FB cavity and lacunae of the funicular cords in the studied species, in particular in B. neritina (Vishnyakov & Ostrovsky, unpublished data), Aquiloniella scabra25 and D. fruticosa (this study). Coelomocytes (and presumed peritoneal cells) with bacteria embedded in their cytoplasm were indeed recorded inside the ooecial vesicle in B. neritina20. Nevertheless, extensive TEM studies of B. neritina ovicells at various stages of placental development (Vishnyakov and Ostrovsky, unpublished data) have not revealed bacteria between placental cells adjoining a developing embryo. The fact that these cells are provided with both tight and adherens junctions (e.g., B. neritina and Bicellariella ciliata73,80), and additionally are covered by a cuticle (albeit thin) raises the question of whether coelomocytes with bacteria and/or bacteria alone can move through the very thick hypertrophied placental epithelium. Interestingly, Miller with co-authors48 detected a gene encoding chitinase in the genome of the symbiont of B. neritina that could potentially be used for cuticle piercing.Another opportunity for the vertical transfer of symbionts is their transport via the supraneural coelomopore during oviposition (see20,81). In this case, free bacteria in the cavity of the maternal zooid could stick to the ovulated oocyte before its transfer into the brood cavity via the coelomopore. However, free bacteria were never recorded in the zooidal cavity. For the Watersipora species, an assumed variant of symbiont transmission is through a strand of mucus extending from the maternal zooid to the released larva and tethering it for a few minutes68.Environmental transmission, when bacteria are acquired from the surrounding seawater, is an alternative option for symbiont acquisition. It may potentially occur either via infection of brooded larvae inside the ovicell by bacteria entering the brood cavity from the external environment or via infection of larvae during the free-swimming period by bacteria from the water column. Published images by Sharp and co-authors40 showed the presence of both symbiotic bacteria and bryostatins both inside the ooecial vesicle and in the peripheral part of the brood cavity, close to the entrance of the ovicell. Although these authors stated that such close “locations of both the bacterial symbionts and the bryostatins demonstrate that the B. neritina–‘E. sertula’ association has a delivery system for both the symbionts and the bryostatins to embryos within the ovicell” (40, p. 699), we argue, based on the above-mentioned data, that this statement remains a probable yet unproven speculation. Our numerous unpublished TEM images indicate the presence of a large number of bacteria filling the brood space between the embryos and the ovicell wall in the brood chambers with and without developing larvae. These bacteria, attracted by some chemical signal(s), can enter the ovicells from outside and infect larvae. Until the transfer of bacteria through the wall of the ooecial vesicle or during oviposition is documented, environmental transmission remains the more probable method. Notably, recent studies on sponge microbiotas showed that the environmental transmission is widespread in this group of suspension feeders82.The hypothesis of external acquisition of bacteria by the bryozoan hosts leaves different infection pathways open. Some of these could potentially develop into vertical transfer. Beyond the infection of larvae, prokaryotes could enter feeding autozooids via the mouth (and further through the intestinal epithelium into the zooidal cavity), through the coelomopore—a presumed entrance for alien sperm76,81,83, or by direct infection of the tentacles (probably by penetration through the outer epithelium).We should stress that FBs were absent in zooidal buds and the youngest zooids with functional polypides in the growing branch tip of one colony of D. fruticosa collected in June. This suggests that bacteria are not transmitted from the older colony parts (and, thus, are not inherited from the founding larvae), but obtained from the external medium since older (and more proximal) zooids had FBs. This idea is supported by the lack of signs of transfer of bacteria between zooids via communication pores and their pore-cell complexes in Dendrobeania fruticosa and Aquiloniella scabra in our TEMs. In contrast, fluorescence microscopy showed symbionts in the non-feeding zooidal bud of the newly-formed small colony of B. neritina40. Bacteria were also present in the preancestrula formed during larval metamorphosis. It remains unknown whether they can move from the preancestrula to the bud along with coelomocytes, with growing funicular cords or both before the formation of transverse walls that isolate newly budded zooids. So, interzooidal transfer to budding sites is possible, and the youngest zooids with functional polypides in the growing tips of D. fruticosa could already receive bacteria too, but FBs were not yet developed. Thus the question of interzooidal/intracolonial transport of bacteria remains open.Two infection pathways—via larvae and by direct penetration through the tissues of the functional polypide, potentially exist in the same species. This is the case in B. neritina, which has morphologically different symbionts in FBs and in the tentacles20. Bacteria in the epithelial wall of the tentacle sheath and ooecial vesicle (see above) could potentially get there via both pathways, or enter the zooid via the coelomopore (third way), subsequently becoming entrapped by coelomocytes or cells of the cystid wall.Finally, the presence of bryozoan sibling species, some of which have symbionts while others do not, and the presence of symbiotic and aposymbiotic colonies within the same species79, suggests that bacteria can be lost and acquired anew at both short- and long-term time scales, as occurs in hermatypic corals and their symbiotic zooxanthellae84,85,86. In this light, it would be important to know whether FBs can develop anew in D. fruticosa after overwintering in the same zooids, or whether they appear only in newly budding zooids. What is the source of bacteria in overwintered colonies? Is it an external infection, or some ‘survivor’-cells (descendants of the bacterial pool from the larva that overwintered inside epithelial cells and/or coelomocytes), or both? This will require further study.Symbiont population dynamics in Dendrobeania fruticosa and its potential driversWhatever the route used by bacteria to enter zooids, they are apparently immediately ‘trapped’ by somatic cells. Free bacteria have never been observed inside the zooidal cavity, another argument against their passage through the wall of the ooecial vesicle to the ovicell.We have shown that regardless of the as-yet-unknown mode of FB development, these temporary organs and the symbionts inside them undergo seasonal changes. Early and mature FBs with non-modified morphology and ‘healthy’ bacteria were found in young zooids only in the colonies collected in June. In one of these colonies, older zooids contained FBs at the initial stage of degradation. In the same month, one colony possessed FBs either at the early-advanced degradation stage (in young zooids) still containing numerous bacteria or at the late-advanced and even terminal stages in old, presumably overwintered zooids. At the initial stage of modification, the slightly developed ‘interlayer’ space between the inner and outer FB cell layers contained fibrils (presumed virus-like particles). Interestingly, the cells of the inner lining apparently engulfed some of the bacterial cells by phagocytosis, supporting our interpretation of the origin of these cells from coelomocytes in this species.One to two months later (August–September), all examined FBs were either at the middle-, or the late-advanced stages of degradation. The number of bacteria in the FB internal cavity distinctly decreased, the inner layer of cells became thinner, and in some regions remained only as a double membrane. The protein-synthesis apparatus was seen only occasionally, and engulfed bacteria were no longer visible inside the inner cells. A wide ILS, formed between the cells of the outer and inner layers, contained abundant putative virus-like particles (Figs. 2, 10). All these FBs were recorded in feeding and non-feeding zooids in the non-growing distal parts of colony branches.Polypide recycling and a seasonal drop of planktonic food alone cannot explain these changes. Firstly, modified FBs were found in zooids with both degenerated and functioning polypides. Secondly, the initial stages of FBs degradation were detected in June when phytoplankton is abundant in the White Sea (e.g.87). We therefore propose the following scenario for the sequence of changes in FBs and their possible causes. In June, newly-formed zooids build funicular bodies containing bacteria that were acquired either from outside or via internal transfer from older colony parts. During that month, FBs begin to degrade. This process continues throughout the rest of the summer. The mid-advanced stage of FB degradation, with few modified bacteria surviving and distributed on the periphery of the FB cavity, was recorded in August. This stage is reminiscent of the final stage in Lutaud’s49 descriptions of the gradual destruction of FBs accompanied by the disappearance of bacterial symbionts in Bugulina turbinata. In late September, FBs change and bacteria disappear, probably through viral lysis (the induction of prophages) (Fig. 2). Young and non-modified FBs were never encountered in August and September, indicating that development of FBs occurs only in young zooids at the growing tips of colony branches in June.Vishnyakov et al.20 recently described the degradation of symbiotic prokaryotes in Bugula neritina and Paralicornia sinuosa accompanied by a change in bacterial morphology similar to bacteriophage-mediated lysis. Degradation process was accompanied by the appearance of polyhedral VLPs in B. neritina and by the formation of structures similar to the so-called metamorphosis-associated contractile complexes (MACs) in P. sinuosa. These complexes are phage-related structures whose activity eventually results in the cell lysis, see88. Although the fate of FBs was not analyzed in their paper, these two VLP variants were observed both inside the bacteria and in the FB internal space by Vishnyakov and co-authors20.In D. fruticosa, presumed VLPs in the form of spherical complexes (as clusters of straight filaments) are present inside bacteria and, together with their fragments, inside the ILS. The filaments were also observed in the free state, frequently curved (apparently flexible) in the internal cavity of FBs. ILS was mostly filled with ‘fibrils’ (potentially representing modified/corrupted filaments) and ‘globules’, although filaments were incidentally recorded inside ILS too. We suggest that, in D. fruticosa, filaments may represent bacteriophage virions. This interpretation is supported by their appearance being associated with the degradation of bacterial cells, as in the case of VLP in B. neritina and P. sinuosa. Nonetheless, the morphology of the spherical complexes built from the filaments in D. fruticosa is unique: they do not resemble any known group of bacterial viruses. We found these putative VLPs inside ILS between the outer and inner FB cell layers. It remains unclear whether they travel there from the FB internal cavity or self-assemble inside ILS from individual filaments that were incidentally met there too. We add that spherical complexes, complete or partial, were recorded inside ILS of the funicular bodies in non-overwintered (collected on 31 September 2019) and presumably overwintered (14 June 2021) zooids.A filamentous morphology is known from only one bacteriophage from the order Tubulavirales, which includes two families Inoviridae and Plectoviridae89. Although inoviruses or plectoviruses have never been reported to assemble in any regular macrocomplexes, the ability of the filamentous Pf phages (inoviruses) of Pseudomonas aeruginosa to form nearly regular liquid crystalline assemblages was recently demonstrated90 (see also review91). Interestingly the formation of such crystals required interactions with bacterial or eukaryotic polymeric molecules such as polysaccharides, DNA and probably mucin90,91.The development of filamentous phages in bacterial cells usually does not kill the cells because these viruses assemble, along with extrusion from the infected bacterium, without disrupting its cell wall (reviewed in92). However, cell death mediated by filamentous prophage induction has been reported in P. aeruginosa due to the emergence of so-called superinfective phage variants93,94,95. Accordingly, the degradation of bacteria in D. fruticosa associated with bacterial viruses is possible.Since the assembly of known filamentous phages is associated with their extrusion from the cell, virions should not accumulate inside bacteria. Although filamentous assembly intermediates may be present (see92), they are not expected to accumulate in such large quantities and/or form superstructures in the bacterial cytoplasm like the ones we found in D. fruticosa (Fig. 9). Our observations revealed nothing resembling the extrusion of a filamentous phage from the surface of a bacterial cell. Therefore, if the described filaments are indeed VLPs, they may represent a new type of bacterial virus.Even though many details remain unknown, we assume that the filaments, ‘globules’, ’fibrils’, and spherical structures in D. fruticosa are of viral origin. Their development following the total disappearance of bacteria in FBs indicates their bacteriophage nature. If so, our observations support the idea that viruses control the number of symbionts in their bryozoan host20, as has been reported in some insects85,86,96. More

Study species and spider collectionAustralomisidia ergandros is a subsocial spider inhabiting South-Eastern Australia. They live in communal kin-groups in nests usually built with leaves from Eucalyptus trees bound by silk threads. Group size usually ranges from 5 to 45 spiderlings. Groups are comprised of the offspring of a single female who provides maternal care until her death28. Offspring continue to live in groups for 5 to 7 months after the mother’s death29,30. One of the females inherit the natal nest while the remaining females disperse to found new nests. It is not entirely clear if A. ergandros inbreed with natal kin or if spiders show a mandatory pre-mating dispersal.We collected 29 A. ergandros nests from a population along Yass River Road in New South Wales, Australia (34° 55′ 20.50′′ S, 149° 6′ 15.53′′ E) in February 2016. At this time of year, the spiderlings are very young and the presence of immigrants, who might influence the extent of social foraging, is improbable9,31. For our experiments, we transferred the original nests to the laboratory at Macquarie University in Sydney.Group composition effectsOur experiments spanned a duration of 56 days. To investigate group composition (cooperators vs. defectors) effects, we first assessed the hunting types of individuals within ‘initial’ groups (phase 1) and subsequently composed and tested ‘sorted’ groups of cooperators or defectors only (phase 2). The formation of initial groups was dictated by special requirements. Basically, we randomly selected up to 30 individuals per original nest and split these individuals into two to three initial groups of ten (Nnests = 10, N groups = 25). Each selected individual received a unique color mark (©Plaka-Farbe) and was weighed to the nearest 0.01 mg on an electronic balance (Mettler Toledo New Classic MS). Each group was then transferred to a petri dish (100 mm in diameter) which served as the test arena for the hunting type assessment. An acclimatization period of four days ensured that the spiders weaved silk threads which amplify vibrations by prey32.Phase 1We assessed hunting types with a modified version of the ‘communal feeding experiment’ originally used by Dumke et al.16 to establish hunting specialization in A. ergandros. For each initial group, we completed 7 feeding trials over 24 days (1 trial every 4 days), during which we offered living Musca domestica flies and observed the foraging behaviour of all group members (Fig. 1). Each fly was weighed before being placed into the petri dish and either removed after two hours if not captured, or after two hours post capture. For each trial, we documented the attack latency, the attacker IDs and the IDs of the feeding individuals in 10-min intervals over two hours. From these data, we determined the feeding frequency of each individual (i.e. the number of trials it was feeding) and calculated the proportions to which it cooperated vs. defected. We thus obtained comparable quantifications of hunting types16. All individuals except those that died during the assessment (56 of 250 spiders) were weighed two days after the last trial to assess weight gain1 (= log (end weight1/start weight133).Phase 2Following phase 1, we regrouped individuals into ‘sorted’ groups of cooperators or defectors only, and this time gave three days acclimatization time since the re-grouping took one day. We formed experimental cooperator groups by selecting nine to ten individuals with the highest cooperating tendencies from the original colony. Next, we formed experimental defector groups analogously from that same pool (Fig. 1). Thus, we achieved paired relatedness between cooperator groups and defector groups, to control for nest origin and nest experience (matched pairs design). We further ensured comparability of cooperator groups and defector groups in the individuals’ physical state (details in Supplementary Methods). Owing to mortality in three nests and restricted possibilities to realize balanced conditions between groups in two nests, we could establish five cooperator-defector group pairs with nine individuals per group.To explore group composition effects on social foraging behaviour and individual fitness payoffs, we tested each sorted group over another seven feeding trials over 24 days. The trials were conducted in exactly the same manner as for the feeding type assessment (phase 1). From the recorded data (attack latency, IDs of attackers, IDs of feeding individuals), we calculated a set of variables that quantified social foraging behaviour (data points per trial and group). To examine individual fitness payoffs, we checked the petri dishes for dead individuals and noted their IDs prior to every trial. As an additional fitness payoff measure for those individuals still alive at the end of phase 2, we determined individual weight gain2 (= log (end weight2/start weight2)).The role of sex in cooperator vs. defector typesTo examine the role of sex in cooperation-defection scenarios, we collected another eight nests from Yass River Road in June 2016. Around this time, A. ergandros individuals reached the subadult stage, at which sex can be visually determined17. Three nests contained subadult males and females in sufficient numbers, so that we formed three groups, each with ten males and ten females from the same nest (in total: N males = 30, N females = 30). All group members were weighed and color marked before they were tested in another, extended feeding type assessment over ten trials.Based on the IDs of attackers and individuals that hunted in these trials, we generated social network graphs and visualized the foraging interactions within groups31,34,35. Individuals were represented by ‘nodes’; a directed line (‘edge’) was drawn from one node to another if the specific individual had cooperated by sharing prey with the other. The lines received weights reflecting the frequency of the respective interaction. We quantified individual prey sharing tendencies using the node-level metric out-strength: the weight sum of all outgoing edges from a particular node35. This metric comprehensively reflects an individual’s prey sharing tendency, as it incorporates the frequency and the spread of prey sharing behaviour. To visualize social networks and calculate the individuals’ out-strengths, we used the software UCINET 636.Statistical analysesAll model analyses were performed in R version 3.2.2, whereas all social network analyses were conducted in UCINET 636.Group composition effectsWe modelled the effect of group composition on social foraging behaviour separately for each response variable with binomial or gamma GEEs (generalized estimation equations). GEEs are adequate to analyse data from repeated measurements over time within same groups because they allow adjustment for the dependence of these measurements37. Defining the dependence structure of our data, we set sorted-group ID as a grouping variable and specified the temporal correlation AR-1. Group composition constituted the explanatory variable of interest, fly weight and group size were included as additional variables to control for prey mass and mortality. An exception was the model for the scrounging degree, in which group size was controlled by the variable itself. We assessed the significance of group composition effects by dropping each explanatory variable in turn and then comparing the full model to its nested models based on Wald test statistics. The least significant variable was removed, and model comparisons were repeated until all remaining variables were significant.Mortality was compared between cooperator groups and defector groups using a Chi-squared test. The difference between group compositions in individual weight gain2 was analysed in a GLS (generalized least squares) model that incorporated an exchangeable correlation structure with sorted-group ID as the grouping variable.Sex differencesWe conducted a node-based Monte Carlo randomization test to determine whether the observed difference in mean out-strength between sexes deviated significantly from the difference expected if producing associations occurred randomly and hence independent of sex. The observed data were shuffled in 10,000 node-label randomizations that preserved group membership. The sum of the differences between mean male out-strength (σm) and mean female out-strength (σf) within groups was used as the test statistic A (A = sumnolimits_{(i = 1)}^{3} {left( {sigma_{{(m_{i} )}} – sigma_{{left( {f_{i} } right)}} } right)}^{ – }), where i denotes group identity. To produce a probability value, we compared the observed test statistic to the distribution of random test statistics drawn from the 10,000 Monte Carlo simulations34. More