Biology subjects

Pruitt, J. N.

Publications and source records attributed to Pruitt, J. N..

12 recordsLinked to original sources

bioRxiv2019

Dispersal behaviour as the outcome and trigger of multilevel selection in a social spider

The facultatively social spider Anelosimus studiosus offers a unique opportunity for understanding how multilevel selection acts in natural populations. However, the importance of previous empirical studies are shaded by a conceptual debate about whether colony-level selection is truly present in these populations or not. Here we introduce a detailed individual based model, where practically all assumptions are supported by empirical data. The only element of the female A. studiosus life cycle missing from the literature is how maturing female spiders decide whether to disperse. This behavioural component we estimate with evolutionary simulations. This model is able to recapitulate the characteristic size and composition distributions of natural populations in different environments. The evolutionary simulations revealed that the optimal dispersal behaviour of a maturing female varies both with her ecological environment and behavioural phenotype. This finding is open for straightforward empirical testing. In agreement with empirical findings we have established parameter ranges where the population is prone to extinction without multiple-female nests. We propose that the dispersal behaviour of individuals is both the result and the prerequisite of multilevel selection in this species.

evolutionary biology↗

bioRxiv2019

Behavioral and physiological evidence that increasing group size ameliorates the impacts of social disturbance

Intra-group social stability is important for the long-term productivity and health of social organisms. We evaluated the effect of group size on group stability in the face of repeated social perturbations using a cooperatively breeding fish, Neolamprologus pulcher. In a laboratory study, we compared both the social and physiological responses of individuals from small versus large groups to the repeated removal and replacement of the most dominant group member (the breeder male). Individuals living in large groups were overall more resistant to instability but were seemingly slower to recover from perturbation. Members of small group were more vulnerable to instability but recovered faster. Breeder females in smaller groups also showed greater physiological preparedness for instability following social perturbations. In sum, we recover both behavioral and physiological evidence that living in larger groups helps to dampen the impacts of social instability in this system.\n\nSO_SCPLOWUMMARYC_SCPLOW SO_SCPLOWTATEMENTC_SCPLOWSocial stability is vital for group productivity and long-term persistence. Here, both behavioral and physiological evidence conveys that larger groups are less susceptible to social disturbance.

animal behavior and cognition↗

bioRxiv2019

Comparative genomics identifies putative signatures of sociality in spiders

Comparative genomics has begun to elucidate the genomic basis of social life in insects but insight into the genomic basis of spider sociality has lagged behind. To begin to characterize genomic signatures associated with the evolution of social life in spiders, we performed one of the first spider comparative genomics studies including five solitary species and two social species, representing two independent origins of sociality in the genus Stegodyphus. We found that the two social spider species had a large expansion of gene families associated with transport and metabolic processes and an elevated genome-wide rate of molecular evolution compared with the five solitary spider species. Genes that were rapidly evolving in the two social species relative to the five solitary species were enriched for transport, behavior, and immune functions, while genes that were rapidly evolving in the solitary species were enriched for energy metabolism processes. Most rapidly evolving genes in the social species S. dumicola were broadly expressed across four tissues and enriched for transport functions, but 12 rapidly evolving genes showed brain-specific expression and were enriched for social behavioral processes. Altogether, our study identifies putative genomic signatures and potential candidate genes associated with spider sociality. These results indicate that future spider comparative genomic studies, including broader sampling and additional independent origins of sociality, can further clarify the genomic causes and consequences of social life.

evolutionary biology↗

bioRxiv2019

Orb-weaving spiders show a correlated syndrome of morphology and web structure in the wild

Extended phenotypes are traits that exist outside the physical body of the organism. Despite their potential role in the lives of both the organisms that express them and other organisms that can be influenced by extended phenotypes, the consistency and covariance with morphological and behaviour traits of extended phenotypes is rarely evaluated, especially in wild organisms. We repeatedly measured an extended phenotype that directly influences an organisms prey acquisition, the web structure, of wild orb-weaving spiders (Micrathena vigorsii), which re-build their webs each day. We related web structure traits to behavioural traits and body size (length). Both web diameter and web density were repeatably different among individuals, while reaction to a predation threat was slightly so, but response to a prey stimulus and web symmetry were not. There was a syndrome between morphology and web structure traits, where larger spiders spun webs that were wider, had webs with increased thread spacing, and the spider tended to react more slowly to a predation threat. When a spider built a relatively larger web it was also relatively a less dense and less symmetrical web. The repeatability of web construction and relationship with spider body size we found may be common features of intra-population variation in web structure in spiders. Individual variation along the morphology and web structure syndrome could represent variation in individual foraging strategies, or age-based correlated changes. By estimating the consistency and covariances of extended phenotypes we can begin to evaluate what maintains their variation and how they might evolve.

animal behavior and cognition↗

bioRxiv2019

Collective behaviour is not robust to disturbance, yet parent and offspring colonies resemble each other in social spiders

Groups of animals possess phenotypes such as collective behaviour, which may determine the fitness of group members. However, the stability and robustness to perturbations of collective phenotypes in natural conditions is not established. Furthermore, whether group phenotypes are transmitted from parent to offspring groups is required for understanding how selection on group phenotypes contributes to evolution, but parent-offspring resemblance at the group level is rarely estimated. We evaluated robustness to perturbation and parent-offspring resemblance of collective foraging aggressiveness in colonies of the social spider Anelosimus eximius. Among-colony differences in foraging aggressiveness were consistent over time but changed if the colony was perturbed through the removal of individuals, or via their removal and subsequent return. Offspring and parent colony behaviour were correlated, but only once the offspring colony had settled after being translocated. The parent-offspring resemblance was not driven by a shared elevation but could be due to other environmental factors. Laboratory collective behaviour was not correlated with behaviour in the field. Colony aggression seems sensitive to initial conditions and easily perturbed between behavioural states. Despite this sensitivity, offspring colonies have collective behaviour that resembles that of their parent colony, provided they are given enough time to settle into the environment.

evolutionary biology↗

bioRxiv2019

Predator-induced selection on urchin activity level depends on urchin body size

Temporally consistent individual differences in behavior impact many ecological processes. We simultaneously examined the effects of individual variation in prey activity level, covering behavior, and body size on prey survival with predators using an urchin-lobster system. Specifically, we tested the hypothesis that slow-moving purple sea urchins (Strongylocentrotus purpuratus) and urchins who deploy extensive substrate (pebbles and stones) covering behavior will out-survive active urchins that deploy little to no covering behavior when pitted against a predator, the California spiny lobster (Panulirus interruptus). We evaluated this hypothesis by first confirming whether individual urchins exhibit temporally consistent differences in activity level and covering behavior, which they did. Next, we placed groups of four urchins in mesocosms with single lobster and monitored urchin survival for 108 hours. High activity level was negatively associated with survival, whereas urchin size and covering behavior independently did not influence survival. The negative effect of urchin activity level on urchin survival was strong for smaller urchins and weaker for large urchins. Taken together, these results suggest that purple urchin activity level and size jointly determine their susceptibility to predation by lobsters. This is potentially of great interest, because predation by recovering lobster populations could alter the stability of kelp forests by culling specific phenotypes, like foraging phenotypes, from urchin populations.

ecology↗

bioRxiv2019

DIVISION OF LABOR INCREASES WITH COLONY SIZE, REGARDLESS OF GROUP COMPOSITION, IN THE SOCIAL SPIDER STEGODYPHUS DUMICOLA

AO_SCPLOWBSTRACTC_SCPLOWDivision of labor (DOL) is a pattern of work organization where individual group members specialize on different tasks. DOL is argued to have been instrumental for the success of eusocial insects, where it scales positively with group size both within and across species. Here we evaluate whether DOL scales positively with group size in a society of cooperative breeders (social spiders) and whether this pattern is impacted by the behavioral composition of the group. To do this we engineered experimental colonies of contrasting group sizes and behavioral compositions and tracked individuals participation in two colony maintenance tasks: prey capture and web construction. As with some eusocial insects, we found that larger groups exhibited DOL metrics up to 10-times greater than smaller groups, conveying that individuals specialize on particular tasks more in larger colonies. This scalar relationship did not differ by a groups behavioral composition, though groups composed of only bold spiders exhibited reduced DOL relative to all-shy or mixed groups. We also found that per capita participation in prey capture, but not web construction, decreased as a function of group size. This suggests that individuals in larger groups may save energy by reducing their involvement in some tasks. Together, our results convey that similar scalar relationships between DOL and group size can emerge both inside and outside the eusocial insects. Thus, theory developed for understanding DOL in eusocial societies may inform our understanding of group function in a larger swath of animal social diversity than is broadly appreciated.\n\nSO_SCPLOWIGNIFICANCEC_SCPLOW SO_SCPLOWTATEMENTC_SCPLOWDivision of labor (DOL) has been a major area of research in the eusocial insects for decades, and is argues to underlie their ecological success. Only recently have other social arthropods, such as social spiders, been considered for studies concerning DOL. Given their smaller colony sizes, and absence of morphological castes, DOL was not thought to be an important facet of spider societies. However, we found that spider societies do indeed exhibit high degrees of DOL that is positively correlated to colony size, as seen in many eusocial insects. These findings suggest that the scalar relationship between group size and social organization seen in social insects is likely generalizable to a larger diversity of social taxa, and that cooperative breeders can show levels of division of labor equaling or exceeding those of eusocial systems evaluated to date.

animal behavior and cognition↗

bioRxiv2019

Multilevel selection in groups of groups

Natural selection occurs at many levels. We evaluated selection acting on collectives at a level of multilevel selection analysis not yet quantified: within and between clusters of groups. We did so by monitoring the performance of natural colonies of social spiders with contrasting foraging aggressiveness in clusters of various sizes. Within-clusters, growth rates were suppressed when colonies were surrounded by more rival groups, conveying that competition is greater. When colonies were surrounded by few rivals, the more aggressive colonies in a cluster were more successful. In contrast, relatively non-aggressive colonies performed better when surrounded by many rivals. Patterns of selection between-clusters depended on the performance metric considered, but cluster-wide aggressiveness was always favored in small clusters. Together, selection both within-and between natural clusters of colonies was detectable, but highly contingent on the number of competing colonies.

evolutionary biology↗

bioRxiv2019

Population differences in aggression are shaped by cyclone-induced selection

Surprisingly little is known about the evolutionary impacts of rare but extreme black swan events, like tropical cyclones. By intercepting three cyclones in fall 2018, we evaluated cyclone-induced selection on collective behavior in a group-living spider. We further examined whether historic frequencies of cyclone landfalls are correlated with geographic variation in group behavior. Cyclones consistently selected for more aggressive spider societies. Furthermore, sites where cyclones have historically been more common also harbor more aggressive groups. Thus, two corroborative lines of evidence convey that that cyclone-induced selection can drive the evolution of colony behavior, and suggest that extreme black swan events can shape within-species diversity and local adaptation.\n\nOne Sentence SummaryTropical cyclones drive the evolution of more aggressive spider societies.

ecology↗

bioRxiv2019

Foundress Number, But Not Queen Size Or Boldness, Predicts Colony Life-History In Wild Paper Wasps

Colonies of social insects exhibit a spectacular variety of life histories. Here we documented the degree of variation in colony life-history traits, mostly related to productivity, in two species of wild paper wasps. We then tested for associations between colony life-history traits to look for trade-offs or positively associated syndromes, and examined whether individual differences in the behavioral tendencies of foundresses (Polistes metricus) or the number of cofoundresses (P. fuscatus) influenced colony life-history. The majority of our measures of colony life-history were positively related, indicating no obvious resource allocation trade-offs. Instead, the positive association of traits into a productivity syndrome appears to be driven by differences in queen or microhabitat quality. Syndrome structure differed only marginally between species. Queen boldness and body size were not associated with colony life-history in P. metricus. Colonies initiated by multiple P. fuscatus foundresses were generally more productive, and this advantage was approximately proportional to the number of cofoundresses. These findings demonstrate that colony life-history traits can be associated together much like individual life-history traits, and the associations seen here convey that differences in overall productivity drive between-colony differences in life-history.

ecology↗

bioRxiv2019

COLLECTIVE AGGRESSIVENESS LIMITS COLONY PERSISTENCE IN HIGH BUT NOT LOW ELEVATION SITES IN AMAZONIAN SOCIAL SPIDERS

Identifying the traits that foster group survival in contrasting environments is important for understanding local adaptation in social systems. Here we evaluate the relationship between the aggressiveness of social spider colonies and their persistence along an elevation gradient using the Amazonian spider, Anelosimus eximius. We found that colonies of A. eximius exhibit repeatable differences in their collective aggressiveness, and that colony aggressiveness is linked with persistence in a site-specific manner. Less aggressive colonies are better able to persist at high-elevation sites, which lack colony-sustaining large-bodied prey, whereas colony aggression was not related to chance of persistence at low-elevation sites. This suggests resistance to resource limitation through docility promotes colony survival at high elevations. These data reveal that the collective phenotypes that relate to colony persistence vary by site, and thus, the path of social evolution in these environments is likely to be affected.

evolutionary biology↗

bioRxiv2019

Resting networks and personality predict attack speed in social spiders

Groups of social predators capture large prey items collectively, and their social interaction patterns may impact how quickly they can respond to time-sensitive predation opportunities. We investigated whether various organizational levels of resting interactions (individual, sub-group, group), observed at different intervals leading up to a collective prey attack, impacted the predation speed of colonies of the social spider Stegodyphus dumicola. We found that in adult spiders overall group connectivity (average degree) increased group attack speed. However, this effect was detected only immediately before the predation event; connectivity two and four days before prey capture had little impact on the collective dynamics. Significantly, lower social proximity of the groups boldest individual to other group members (closeness centrality) immediately prior and two days before prey capture was associated with faster attack speeds. These results suggest that for adult spiders, the long-lasting effects of the boldest individual on the groups attack dynamics are mediated by its role in the social network, and not only by its boldness. This suggests that behavioural traits and social network relationships should be considered together when defining keystone individuals in some contexts. By contrast, for subadult spiders, while the group maximum boldness was negatively correlated with latency to attack, no significant resting network predictors of latency to attack were found. Thus, separate behavioural mechanisms might play distinctive roles in determining collective outcomes at different developmental stages, timescales, and levels of social organization.\n\nSignificance statementCertain animals in a group, such as leaders, may have a more important role than other group members in determining their collective behavior. Often these individuals are defined by their behavioral attributes, for example, being bolder than others. We show that in social spiders both the behavioral traits of the influential individual, and its interactions with other group members, shape its role in affecting how quickly the group collectively attacks prey.

animal behavior and cognition↗