Animal Personality Aligns Task Specialization and Task Proficiency in a Spider Society,” by Colin M
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Editorial Expression of Concern ECOLOGY PNAS is publishing an Editorial Expression of Concern regarding the following article: “Animal personality aligns task specialization and task proficiency in a spider society,” by Colin M. Wright, C. Tate Holbrook, and Jonathan N. Pruitt, which was first pub- lished June 16, 2014; 10.1073/pnas.1400850111 (Proc. Natl. Acad. Sci. U.S.A. 111, 9533–9537). The editors wish to alert readers of an ongoing investigation by McMaster University into the underlying data of this work. We will await the conclusion of the investigation to determine whether further action is required. Published under the PNAS license. First published May 7, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2008526117 11844 | PNAS | May 26, 2020 | vol. 117 | no. 21 www.pnas.org Downloaded by guest on September 23, 2021 Animal personality aligns task specialization and task proficiency in a spider society Colin M. Wrighta,1, C. Tate Holbrookb, and Jonathan N. Pruitta aDepartment of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260; and bDepartment of Natural Sciences, College of Coastal Georgia, Brunswick, GA 31520 Edited by Raghavendra Gadagkar, Indian Institute of Science, Bangalore, India, and approved May 19, 2014 (received for review January 16, 2014) Classic theory on division of labor implicitly assumes that task contexts, also may be important in orchestrating division of labor specialists are more proficient at their jobs than generalists and (15, 17, 18); however, our understanding of how animal per- specialists in other tasks; however, recent data suggest that this sonality maps onto conventional theory of social organization, might not hold for societies that lack discrete worker polymor- and division of labor in particular, is still in its infancy. phisms, which constitute the vast majority of animal societies. The Division of labor is generally thought to enhance colony per- facultatively social spider Anelosimus studiosus lacks castes, but formance and ultimately fitness. Theoretically, benefits may be females exhibit either a “docile” or “aggressive” phenotype. Here realized at the level of individual specialists and/or through we observed the propensity of individual females of either phe- colony-level efficiencies in the organization of work (1, 9). In- notype to perform various tasks (i.e., prey capture, web building, dividuals specializing in certain tasks may be more proficient at parental care, and colony defense) in mixed-phenotype colonies. those tasks if they have corresponding innate ability or aptitude, We then measured the performance outcomes of singleton indi- which may have morphological or physiological correlates (4, viduals of either phenotype at each task to determine their profi- 19), or if learning/experience improves their task-related skills ciencies. Aggressive females participated more in prey capture, (20, 21). For individuals, proficiency at one task might not web building, and colony defense, whereas docile females en- translate into proficiency at another task (i.e., transfer), and can gaged more in parental care. In staged trials, aggressive individu- result in a reduction in an individual’s ability to perform other als were more effective at capturing prey, constructing webs, and tasks (i.e., interference), which then favors societies in which ECOLOGY defending the colony, whereas docile females were more effective individuals perform only one task or a restricted number of tasks at rearing large quantities of brood. Thus, individuals’ propensity within a colony (22, 23). Additional colony-level benefits of di- to perform tasks and their task proficiencies appear to be adap- vision of labor may include a more streamlined flow of materials tively aligned in this system. Moreover, because the docile/aggres- within a colony (24) and faster responses to variable work de- sive phenotypes are heritable, these data suggest that within- mands, perhaps facilitated by the spatial organization of indi- colony variation is maintained because of advantages gleaned viduals and tasks. by division of labor. Here we focus on individual-level task proficiency, which we operationally define and measure based on relative differences behavioral syndrome | social organization | cooperation | temperament | in the performance outcomes of a task, whether related to innate Araneae aptitude or to learning gains. Many studies on division of labor have tacitly assumed a priori that individuals specializing in ivision of labor is a pattern of specialization by cooperative certain tasks actually perform these tasks better than specialists Dindividuals who perform different tasks and/or roles in a of another task or generalists. That hypothesis has rarely been society (1). Although the concept originally arose in reference tested, however. An exception is the case of social insects with to human assembly workers, scientists now use the term to de- polymorphic workers, when sheer size or specialized morphology scribe task differentiation in a variety of animal societies. The can enhance individual performance of nest defense, debris re- classic study systems for division of labor are eusocial insects, moval, foraging, or parental care (2, 15, 25). Some of the very such as ants, bees, wasps, and termites, which exhibit nonre- productive division of labor in the following three forms: (i) Significance polymorphisms among worker castes (subcastes), such as those described in several ant species (e.g., leaf-cutter ants) (2–4); (ii) Here we demonstrate strong links among task specialization, age-dependent task differentiation, known as age or temporal task proficiency, and animal personality in a nonpolymorphic polyethism (5), as seen in honey bees (6); and (iii) task differ- spider, reminiscent of the associations observed among task entiation in the absence of morphological variation within a caste specialization, task aptitude, and castes in the social insects. (7–9). The latter pattern likely is the most broadly occurring not Such links previously have been demonstrated only for single only in social insects, most of which lack worker polymorphism, tasks, and some studies failed to find any links whatsoever. In but also in a diverse array of other social taxa (10, 11), and it may contrast, the present study demonstrates such links in four even emerge at the origin of sociality (12). different tasks important for proper colony function. Unlike Division of labor is widely understood as a self-organizing or morphological castes, individual differences in personality emergent property that arises from local interactions among have been detected in almost every animal system imaginable. group members and their shared environment (13). Various Thus, we argue that the classic canon of theories and pre- models have been developed to explain this process in social dictions developed in the context of castes could be adaptively insects, many invoking interindividual variation in responsiveness retrofitted and redeployed in the personality literature to a to task-related stimuli (14, 15). Response-threshold variation much broader swath of animal diversity. and subsequent task differentiation may be mediated by a mul- titude of mechanisms including, but not limited to, genotype, Author contributions: J.N.P. designed research; J.N.P. performed research; C.M.W. and gene expression, hormonal and other physiological changes, C.T.H. analyzed data; and C.M.W. wrote the paper. learning and early life experience, spatial heterogeneity, and The authors declare no conflict of interest. group size (16). More recently, it has been suggested that animal This article is a PNAS Direct Submission. personality, or consistent variation in individual behavior across 1To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1400850111 PNAS Early Edition | 1of5 limited number of studies in nonpolymorphic social insects have demonstrated superior performance by task specialists (20, 26–28), whereas others have found no relationship between task specialization and measures of individual proficiency (9, 29). Thus, more studies are needed to explore the potential link be- tween task specialization and task proficiency, particularly in so- cieties lacking discrete worker polymorphisms, which constitute the vast majority of animal societies (including social insects). Anelosimus studiosus (Araneae, Theridiidae) is a social spider that, like all other social spiders, does not exhibit discrete morphological castes (30). Instead, individual females display a discrete, bimodal behavioral polymorphism of “docile” and “aggressive” behavioral types (31, 32). Aggressive females show heightened aggression and responsiveness toward predators, prey, and mates (33–36). In this species, individual differences in behavior or “personality” are thought to play an organizing role analogous to that of castes in social insects. Consistent with this hypothesis, studies of mixed- phenotype colonies have shown that aggressive females are more likely than docile females to attack prey and colony invaders (37, 38). Furthermore, colonies of mixed phenotype outperform colonies of purely docile or purely aggressive females (37, 39), possibly because of division of labor. The foregoing findings cannot address whether or not aggressive females are performing particular tasks at which they are more proficient than docile females, however, and we do not have a good understanding of the roles played by docile females