The Ecology of Spider Sociality: A Spatial Model.

AbstractThe emergence of animal societies offers unsolved problems for both evolutionary and ecological studies. Social spiders are especially well suited to address this problem given their multiple independent origins and distinct geographic distribution. On the basis of long-term research on the spider genus Anelosimus, we developed a spatial model that re-creates observed macroecological patterns in the distribution of social and subsocial spiders. We show that parallel gradients of increasing insect size and disturbance (rain, predation) with proximity to the lowland tropical rain forest would explain why social species are concentrated in the lowland wet tropics but absent from higher elevations and latitudes. The model further shows that disturbance, which disproportionately affects small colonies, not only creates conditions that require group living but also tempers the dynamics of large social groups. Similarly simple underlying processes, albeit with different players on a somewhat different stage, may explain the diversity of other social systems.

Kleptoparasites of social spider colonies do not track hosts' subdivided population structure.

Organisms with lower dispersal abilities tend to have more genetically dissimilar populations. The same is true for parasites, whose transmission frequency may depend on the population structure of the host. This should be especially true when hosts and parasites face similar barriers to dispersal. Here, we considered the similarities between host and parasite population structure in a social spider system. In this system, host colonies are typified by rapid growth via internal recruitment followed by budding or fission events when colonies grow too large, with each colony representing a distinct population. Host colonies provide habitat for kleptoparasitic spiders, which steal prey from and may also feed directly on host individuals. We asked whether kleptoparasites exhibit a similar degree of population subdivision as their host. Under the free-mixing hypothesis (i.e., horizontal transmission), kleptoparasites would have well-mixed populations across broader regions than a single host nest, whereas host populations would be strongly genetically structured. Under the host-tracking hypothesis (i.e., vertical transmission), kleptoparasites would have a population structure that parallels that of the host. We conducted a genotype-by-sequencing study to assess the population structure of both hosts and kleptoparasites within three nearby regions in eastern Ecuador. We found strong signatures of population differentiation and bottlenecks in the host species, which is congruent with past studies. However, we found that kleptoparasite populations were well mixed across host nests, with no evidence of recent bottlenecks. These results support our free-mixing hypothesis, suggesting that kleptoparasites follow patterns of horizontal transmission in this social spider system.

Economies of scale shape energetics of solitary and group-living spiders and their webs.

Metabolic scaling, whereby larger individuals use less energy per unit mass than smaller ones, may apply to the combined metabolic rate of group-living organisms as group size increases. Spiders that form groups in high disturbance environments can serve to test the hypothesis that economies of scale benefit social groups. Using solitary and group-living spiders, we tested the hypothesis that spiders exhibit negative allometry between body or colony mass and the standing mass of their webs and whether, and how, such a relationship may contribute to group-living benefits in a cooperative spider. Given the diverse architecture of spider webs-orb, tangle and sheet-and-tangle, and associated differences in silk content, we first assessed how standing web mass scales with spider mass as a function of web architecture and whether investment in silk differs among web types. As group-living spiders are predominantly found in clades that build the presumably costlier sheet-and-tangle webs, we then asked whether cost-sharing through cooperative web maintenance contributes to a positive energy budget in a social species. We found that larger spiders had a relatively smaller investment in silk per unit mass than smaller ones, but more complex sheet-and-tangle webs contained orders of magnitude more silk than simpler orb or tangle ones. In the group-living species, standing web mass per unit spider mass continued to decline as colony size increased with a similar slope as for unitary spiders. When web maintenance activities were considered, colonies also experienced reduced mass-specific energy expenditure with increasing colony size. Activity savings contributed to a net positive energy balance for medium and large colonies after inputs from the cooperative capture of large prey were accounted for. Economies of scale have been previously demonstrated in animal societies characterized by reproductive and worker castes, but not in relatively egalitarian societies as those of social spiders. Our findings illustrate the universality of scaling laws and how economies of scale may transcend hunting strategies and levels of organization.

Cylindropuntia cholla aqueous root rich in phytosterols enhanced immune response and antimicrobial activity in tilapia Oreochromis niloticus leukocytes.

"Cacti" are rich sources of phytochemicals with antioxidant activity, and their use is mainly focused on infusions in traditional medicine in Mexico. This study characterizes the chemical compounds found in Cylindropuntia cholla root by gas chromatography coupled to mass spectrometry (GC-MS) and determines the total content of polyphenols and flavonoids, as well as their antioxidant capacity. The immunostimulatory effect of aqueous C. cholla root extract (ACcr) was evaluated at concentrations of 50, 250, 500, and 1000 µg/mL in Tilapia peripheral blood leukocytes. The results obtained by the GC-MS analysis revealed the presence of phenolic acids, flavonoid and phytosterol derivatives as ß-sitosterol and campesterol. The determination of the total polyphenol and flavonoid contents indicated that ACcr is abundant in polyphenols, showing an anti-radical capacity of scavenging free radicals, such as those of hydroxyl and superoxide, as well as an increase in lipid peroxidation inhibition capacity. Stimulation of tilapia leukocytes resulted in the increase of its phagocytic activity, respiratory burst, nitric oxide production, and superoxide dismutase activity. Finally, the results obtained for the first time allowed establishing the chemical profile of ACcr and its antimicrobial activity against three important pathogenic bacteria. The potential of this root is indicated as an additive in formulating antioxidant and immunostimulant supplements for the aquaculture and pharmaceutical industry.

Resource exchange and partner recognition mediate mutualistic interactions between prey and their would-be predators.

Animals may develop mutualistic associations with other species, whereby prey offer resources or services in exchange for protection from predators. Alternatively, prey may offer resources or services directly to their would-be predators in exchange for their lives. The latter may be the case of hemipterans that engage in mutualistic interactions with ants by offering a honeydew reward. We test the extent to which a honeydew offering versus partner recognition may play a role as proximate mechanisms deterring ants from predating upon their hemipteran partners. We showed that, when presented with a choice between a hemipteran partner and an alternative prey type, mutualist ants were less likely to attack and more likely to remain probing their hemipteran partners. This occurred even in the absence of an immediate sugary reward, suggesting either an evolved or learned partner recognition response. To a similar extent, however, ants were also less likely to attack the alternative prey type when laced with honey as a proxy for a honeydew reward. This was the case even after the honey had been depleted, suggesting an ability of ants to recognize new potential sources of sugars. Either possibility suggests a degree of innate or learned partner recognition.

Trait overdispersion and the role of sociality in the assembly of social spider communities across the Americas.

Among the factors that may lead to differences in resource use among closely related species, body size and morphology have been traditionally considered to play a role in community assembly. Here we argue that for animals that live and forage in groups, level of sociality, reflecting differences in group size and cooperative tendencies, can be an additional and powerful dimension separating species in niche space. We compare 50+ communities of the social spider genus Anelosimus across the Americas against a null model that accounts for known effects of biotic and abiotic factors on the distribution of social systems in the genus. We show that these communities are more overdispersed than expected by chance in either or both body size and level of sociality, traits we have previously shown to be associated with differences in resource utilization (prey size, microhabitat, and phenology). We further show that the contribution of sociality to differences in the size of the prey captured is two to three times greater than that of body size, suggesting that changes in group size and cooperative tendencies may be more effective than changes in body size at separating species in niche space.

Decreasing Predator Density and Activity Explains Declining Predation of Insect Prey along Elevational Gradients.

Predation, which is a fundamental force in ecosystems, has been found to decrease in intensity with elevation and latitude. The mechanisms behind this pattern, however, remain unaddressed. Using visual sampling of potential predators and live flies as baits, we assessed predation patterns along 4,000-m elevation transects on either side of the equatorial Andes. At the lower elevations, we found that around 80% of predation events on our insect baits were due to ants. The decline in predation with elevation was driven mainly by a decline in the abundance of ants, whose importance relative to other predators also declined. We show that both predator density and activity (predation rate per individual predator) decreased with elevation, thus ascribing specific mechanisms to known predation patterns. We suggest that changes in these two mechanisms may reflect changes in primary productivity and metabolic rate with temperature, factors of potential relevance across latitudinal and other macroecological gradients, particularly for ectotherm predators and prey.

Female-Biased Sex Ratios Increase Colony Survival and Reproductive Output in the Spider Anelosimus studiosus.

Negative frequency-dependent selection acting on the sexes is hypothesized to drive populations toward a balanced sex ratio. However, numerous examples of female-biased sex ratios pepper the arthropods. Theoretical examinations have proposed that female-biased populations or groups can have higher chances of surviving and propagating that may be advantageous. We evaluated this hypothesis in the semisocial spider Anelosimus studiosus by creating artificial colonies of varying sex ratios and sizes and observing colony performance at sites with high versus low group extinction rates. We also tested whether colony extinction rates and sex ratios were correlated across 25 collection sites, spanning 10° latitude. We found that colonies with female-biased sex ratios produced more egg cases and were more likely to survive the duration of a field season, suggesting that female-biased sex ratios confer both survival and reproductive advantages on colonies. The effect of sex ratio on colony survival and reproductive output was strongest for small colonies in high extinction areas. Moreover, we found that female-biased sex ratios correlated with greater extinction rates across 25 sites, indicating that female-biased sex ratios may have evolved at some sites in response to high extinction rates. These findings suggest that selection favoring groups with female-biased sex ratios may operate in A. studiosus, shedding light on some of the factors that may drive the evolution of biased sex ratios.

Prey size and scramble vs. contest competition in a social spider: implications for population dynamics.

There are many benefits of group living, but also substantial costs, one of which is competition for resources. How scarce food resources are distributed among different members of a population or social group - whether via scramble or contest competition - can influence not only the variance in individual fitness, but also the stability and therefore survival of the group or population. Attributes of the food resources themselves, such as their size, may influence the type of intraspecific competition that occurs and therefore the intrinsic stability of a group or population. By experimentally manipulating the size of prey fed to artificial colonies of the social spider Anelosimus eximius, we investigated whether prey size could alter the degree of scramble vs. contest competition that takes place and, thus, potentially influence colony population dynamics. We found that large prey were shared more evenly than small prey and that individuals in poor condition were more likely to feed when prey were large than when prey were small. Additionally, we show that individuals participating in prey capture are also more likely to feed on the captured prey. We developed a simple mathematical model to explore the prey sizes that would be energetically worth defending, i.e. prey that are 'economically defendable'. The model shows that neither very small prey, nor prey above a certain size is worth monopolizing, with only intermediate size prey being 'economically defendable'. We therefore suggest the small and large prey in our experiment corresponds to our model's intermediate and large prey categories, respectively. As the size of prey captured by social spider colonies increases with colony size, our findings suggest that scramble competition may predominate in large colonies. Scramble competition, combined with the fact that prey biomass per capita declines as colonies grow beyond a certain size, would then explain why extremely large colonies of this social spider may suddenly go extinct. Our project thus illustrates the potential triple link between characteristics of the resources, individual behaviour and population dynamics, a link rarely considered in an empirical setting.

Community-wide body size differences between nocturnal and diurnal insects.

Examining community-wide patterns for the most diverse animal group, insects, is fundamental to our understanding of the ecological and evolutionary factors that maintain tropical diversity. Using several sampling techniques (malaise traps, pitfall traps, visual searches, and social spider nest captures), we investigated the day-night community composition of active insects to reveal differences in body size at three elevations in eastern Ecuador. We show that insects active at night are, on average, larger than those active during the day. Even though insect size decreased with increasing elevation, the observed diel pattern was consistent across elevations, and for most insect orders. All sampling techniques consistently detected day--night differences in insect size, except for social spider captures at the two higher elevations, probably due to the reduced range of colony sizes at the higher elevations and possibly lower spider activity at night. We suggest that the observed diel patterns in insect size may be driven by a combination of factors, including increased risk imposed on large insects by diurnal visual predators, mainly insectivorous birds, and physiological responses to diel changes in abiotic conditions.

Differences in group size and the extent of individual participation in group hunting may contribute to differential prey-size use among social spiders.

We have previously shown that the range of prey sizes captured by co-occurring species of group-hunting social spiders correlates positively with their level of sociality. Here, we show that this pattern is probably caused by differences among species in colony size and the extent to which individuals participate in group hunting. We assess levels of participation for each species from the fraction of individuals responding to the struggling prey that partake as attackers and from the extent to which the number of attackers increases with colony size. Of two species that form equally large colonies, the one that captures on average larger prey engaged as attackers a significantly larger fraction of individuals that responded to struggling prey and also increased its number of attackers in larger colonies when presented with large prey items. Surprisingly, a third co-occurring species previously found to capture smaller insects than the other two exhibited the highest levels of participation. This species, however, typically forms small single-family colonies, thereby being limited in the size of insects it can capture. It is thus a combination of colony size and the extent of individual participation (or cooperation) that probably determines patterns of resource use in this community of co-occurring social predators.

Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous.

The evolution of group living is regarded as a major evolutionary transition and is commonly met with correlated shifts in ancillary characters. We tested for associations between social tendency and a myriad of abiotic variables (e.g., temperature and precipitation) and behavioral traits (e.g., boldness, activity level, and aggression) in a clade of spiders that exhibit highly variable social structures (genus Anelosimus). We found that, relative to their subsocial relatives, social species tended to exhibit reduced aggressiveness toward prey, increased fearfulness toward predators, and reduced activity levels, and they tended to occur in warm, wet habitats with low average wind velocities. Within-species variation in aggressiveness and boldness was also positively associated with sociality. We then assessed the functional consequences of within-species trait variation on reconstituted colonies of four test species (Anelosimus eximius, Anelosimus rupununi, Anelosimus guacamayos, and Anelosimus oritoyacu). We used colonies consisting of known ratios of docile versus aggressive individuals and group foraging success as a measure of colony performance. In all four test species, we found that groups composed of a mixture of docile and aggressive individuals outperformed monotypic groups. Mixed groups were more effective at subduing medium and large prey, and mixed groups collectively gained more mass during shared feeding events. Our results suggest that the iterative evolution of depressed aggressiveness and increased within-species behavioral variation in social spiders is advantageous and could be an adaptation to group living that is analogous to the formation of morphological castes within the social insects.

Co-evolution between sociality and dispersal: the role of synergistic cooperative benefits.

Explaining the evolution of sociality is challenging because social individuals face disadvantages that must be balanced by intrinsic benefits of living in a group. One potential route towards the evolution of sociality may emerge from the avoidance of dispersal, which can be risky in some environments. Although early studies found that local competition may cancel the benefits of cooperation in viscous populations, subsequent studies have identified conditions, such as the presence of kin recognition or specific demographic conditions, under which altruism will still spread. Most of these studies assume that the costs of cooperating outweigh the direct benefits (strong altruism). In nature, however, many organisms gain synergistic benefits from group living, which may counterbalance even costly altruistic behaviours. Here, we use an individual based model to investigate how dispersal and social behaviour co-evolve when social behaviours result in synergistic benefits that counterbalance the relative cost of altruism to a greater extent than assumed in previous models. When the cost of cooperation is high, selection for sociality responds strongly to the cost of dispersal. In particular, cooperation can begin to spread in a population when higher cooperation levels become correlated with lower dispersal tendencies within individuals. In contrast, less costly social behaviours are less sensitive to the cost of dispersal. In line with previous studies, we find that mechanisms of global population control also affect this relationship: when whole patches (groups) go extinct each generation, selection favours a relatively high dispersal propensity, and social behaviours evolve only when they are not very costly. If random individuals within groups experience mortality each generation to maintain a global carrying capacity, on the other hand, social behaviours spread and dispersal is reduced, even when the latter is not costly.

Genomic signatures of recent convergent transitions to social life in spiders.

The transition from solitary to social life is a major phenotypic innovation, but its genetic underpinnings are largely unknown. To identify genomic changes associated with this transition, we compare the genomes of 22 spider species representing eight recent and independent origins of sociality. Hundreds of genes tend to experience shifts in selection during the repeated transition to social life. These genes are associated with several key functions, such as neurogenesis, behavior, and metabolism, and include genes that previously have been implicated in animal social behavior and human behavioral disorders. In addition, social species have elevated genome-wide rates of molecular evolution associated with relaxed selection caused by reduced effective population size. Altogether, our study provides unprecedented insights into the genomic signatures of social evolution and the specific genetic changes that repeatedly underpin the evolution of sociality. Our study also highlights the heretofore unappreciated potential of transcriptomics using ethanol-preserved specimens for comparative genomics and phylotranscriptomics.

Cooperative capture of large prey solves scaling challenge faced by spider societies.

A decrease in the surface area per unit volume is a well known constraint setting limits to the size of organisms at both the cellular and whole-organismal levels. Similar constraints may apply to social groups as they grow in size. The communal three-dimensional webs that social spiders build function ecologically as single units that intercept prey through their surface and should thus be subject to this constraint. Accordingly, we show that web prey capture area per spider, and thus number of insects captured per capita, decreases with colony size in a neotropical social spider. Prey biomass intake per capita, however, peaks at intermediate colony sizes because the spiders forage cooperatively and larger colonies capture increasingly large insects. A peaked prey biomass intake function would explain not only why these spiders live in groups and cooperate but also why they disperse only at large colony sizes, thus addressing both sociality and colony size range in this social spider. These findings may also explain the conspicuous absence of social spiders from higher latitudes and higher elevations, areas that we have previously shown to harbor considerably fewer insects of the largest size classes than the lowland tropical rainforests where social spiders thrive. Our findings thus illustrate the relevance of scaling laws to the size and functioning of levels of organization above the individual.

Population differences in behaviour are explained by shared within-population trait correlations.

Correlations in behavioural traits across time, situation and ecological context (i.e. 'behavioural syndromes' or 'personality') have been documented for a variety of behaviours, and in diverse taxa. Perhaps the most controversial inference from the behavioural syndromes literature is that correlated behaviour may act as an evolutionary constraint and evolutionary change in one's behaviour may necessarily involve shifts in others. We test the two predictions of this hypothesis using comparative data from eighteen populations of the socially polymorphic spider, Anelosimus studiosus (Araneae, Theriidae). First, we ask whether geographically distant populations share a common syndrome. Second, we test whether population differences in behaviour are correlated similarly to within-population trait correlations. Our results reveal that populations separated by as much as 36 degrees latitude shared similar syndromes. Furthermore, population differences in behaviour were correlated in the same manner as within-population trait correlations. That is, population divergence tended to be along the same axes as within-population covariance. Together, these results suggest a lack of evolutionary independence in the syndrome's constituent traits.

It takes grouping and cooperation to get sociality.

Cooperation and grouping are regularly studied as separate traits. The evolution of sociality however requires both that individuals get together in groups and that they cooperate within them. Because the level of cooperation can influence selection for group size, and vice versa, it is worth studying how these traits coevolve. Using a generally applicable two-trait optimization approach, we provide analytical solutions for three specific models. These solutions describe how cooperative associations of non-relatives evolve, and predict how large and how cooperative they will be. The analytical solutions help understand how changes in parameter values, such as the group carrying capacity and the costs of cooperation, affect group size and the level of cooperation in equilibrium. Although the analytical model makes a few simplifying assumptions-populations are assumed to be monomorphic for grouping as well as for cooperative tendencies, and group size is assumed to be deterministic-simulations show that its predictions are matched quite closely by results for settings where these assumptions do not hold.

Gradients of precipitation and ant abundance may contribute to the altitudinal range limit of subsocial spiders: insights from a transplant experiment.

Species range boundaries often form along environmental gradients that dictate the success of the phenotypes present in each habitat. Sociality may allow colonization of environments where related species with a solitary lifestyle cannot persist. Social spiders in the genus Anelosimus appear restricted to low- and mid-elevation moist environments in the tropics, while subsocial spiders, common at higher elevations and latitudes, appear to be absent from the lowland tropical rainforest. Here, we seek factors that may simultaneously prevent subsocial Anelosimus species from colonizing the lowland rainforest while favouring species with large social groups in this habitat. To this end, we transplanted small groups of a subsocial species, which contain the offspring of a single female, from cloud forest habitat in the centre of its natural range to lower montane rainforest on the range margin and to lowland rainforest outside of the species range. Groups transplanted at the range margin and below their range limit were less likely to disperse and experienced increased mortality. This was correlated with greater rainfall intensity and ant abundance. We show that protection from rainfall enhances the performance of small groups of spiders in the lowland rainforest, and suggest that predation or disturbance by ants may influence the geographical range limits of this species.