3 THE EVOLUTION AND DEVELOPMENT OF EUSOCIAL INSECT BEHAVIOR Adam G. Dolezal , 1 Kevin B. Flores , 1 Kirsten S. Traynor , 1 and Gro V. Amdam 1,2 1 School of Life Sciences , Arizona State University , Tempe , AZ 2 Department of Chemistry, Biotechnology and Food Science , University of Life Sciences , Aas , Norway THE PATH FROM SOLITARY LIFE TO ADVANCED SOCIAL LIVING Eusociality: Defi ning the Extremes of Social Life Many different organisms exhibit social behavior. These behaviors are sometimes defi ned as interactions between two or more members of a species, but then most sexually repro- ducing animals would behave socially. With social behavior, we refer to phenotypes in animals that live in conspecifi c groups. The most advanced forms of such groups are found among the eusocial insects, which include ants, bees, wasps, and termites. Like human societies, eusocial insects engage in agriculture, warfare, and communicate via abstract language, and, in sheer numbers and mass, they dominate the insect world. We often think of grass-eating mammals as the major herbivores, but leaf-cutter ants process more green- ery in the Neotropics and the southwestern deserts of the United States, and harvester ants have as voracious an appetite for seeds as mammals ( Gullan and Cranston 2000 ). The high level of success and diversity enjoyed by eusocial organisms can be attrib- uted to their unique adaptations to life. But how do eusocial species differ from those that simply are social? The eusocials exhibit three characteristics that set them apart from other social species: Advances in Evolutionary Developmental Biology, First Edition. Edited by J. Todd Streelman. © 2014 John Wiley & Sons, Inc. Published 2014 by John Wiley & Sons, Inc. 37 38 THE EVOLUTION AND DEVELOPMENT OF EUSOCIAL INSECT BEHAVIOR 1. Reproductive division of labor: only one or a few individuals monopolize the production of offspring. 2. Cooperative care of young: helper individuals called workers care for their siblings, instead of reproducing. 3. Overlapping generations: parents and offspring share the same nest and raise mul- tiple batches of young. Such exceptionally organized societies can outcompete solitary individuals in many scenarios. Solitary insects must fi nd nesting sites, forage, and reproduce consecutively, engaging at only one task at a time, and are frequently exposed to predation and environ- mental stresses (Wilson 1990). Eusocial colonies can engage in all tasks simultaneously and keep the majority of their members effi ciently protected, making them highly produc- tive. Yet the organization of large societies required the evolution of many traits, including task specializations and task plasticities driven by genetic or epigenetic regulation. In most species, natural selection for such traits was either not suffi ciently strong or suffi ciently possible based on available and selectable variation. Thus, only a few evolved eusociality. Some other species represent intermediate levels of social organization, living in com- munal or subsocial groups ( Hölldobler and Wilson 2009 ). In this chapter, we look at social insects within an evolutionary developmental bio logy perspective. With this approach, it is possible to study behavioral development and evolu- tion in a variety of species to understand how social behaviors evolved from solitary ancestral states. By treating behavioral traits as modules, similar to modules described in morphological development, insight can be gained into how gene regu latory networks were rearranged during evolution ( Robinson et al. 2005 ; Toth and Robinson 2007 ). Euso- ciality is found in several insect taxa, but the best-studied groups are in the order Hyme- noptera that includes bees, ants, and wasps. The majority of recent advancements in understanding the evolution of development in social insect behavioral evolution occurred in Hymenopterans, and thus, they provide the focus of this text. The Starting Point: A Solitary Life Cycle Extant solitary insects can be used to extract information about the path from solitary to eusocial life. The life cycle of the solitary leaf-cutter bee, Megachile rotunda , is an illustration of a typical solitary, provisioning bee. The adults emerge during summer after diapause—a period of dormancy and arrested development—and immediately mate ( Pitts-Singer and Cane 2011 ). They then forage for carbohydrate-rich food, gath- ering nectar from fl owers for energy. To activate their ovaries for production of eggs, females eat protein-rich pollen. Each female then builds a nest in a preexisting, aboveg- round fi ssure ( Kemp and Bosch 2000 ) and constructs a single-fi le row of cells ( Pitts- Singer and Cane 2011 ). When the female departs to forage for food or building materials, she leaves her nest unattended and undefended. Into each cell, she hoards a mixture of pollen and some nectar before she lays a single egg on top of the resource. Within a few days the egg hatches, and the larva consumes the food stores before it pupates and metamorphosis occurs. Instead of completing development and emerging as an adult, some M. rotunda enter diapause as a prepupa—effectively postponing maturation until next summer when the cycle begins again ( Pitts-Singer and Cane 2011 ; Figure 3.1 A). A B Figure 3.1. Solitary versus eusocial life cycle. (A) In the solitary bee, exemplifi ed here by Mega- chile rotunda , an individual female must sequentially perform all tasks necessary for reproduc- tion, raising only one offspring at a time. At any point, the bee and her nest are exposed to predatory risk (green background). (B) In the eusocial insects, exemplifi ed here by the honeybees ( Apis mellifera ), reproductive and nonreproductive tasks have been split into separate castes. The queen (crown) produces many offspring, while workers transition across tasks over time. The terminal stage of a worker ’ s life is usually foraging, during which many bees have individual food collection preferences (nectar vs. pollen). Compared to a solitary bee, honeybees are exposed to predation for much less of their lives (green background). 40 THE EVOLUTION AND DEVELOPMENT OF EUSOCIAL INSECT BEHAVIOR Figure 3.2. Insect aggregations. Many insect species form aggregations without being eusocial. From left to right: Monarch butterfl ies ( Nanaus plexippus) form large groups for overwintering; Japanese beetles ( Popillia japonica) , brown marmorated stink bugs ( Halyomorpha halys ), and locust swarms (Acrididae) aggregate around common food sources. Aggregations For complex societies to evolve, individuals must fi rst come in contact as groups ( Gadau et al. 2009 ). Aggregations act as the starting point for these trajectories and exemplify the simplest form of social behavior. Aggregations are groups only in the sense that they are associations of individuals living at a higher density than in surrounding areas ( Camazine 2001 ). Aggregations can form for mating purposes, mutual defense, or simply around an important resource (Figure 3.2 ). Therefore, aggregations of insects do not necessarily involve many of the traits observed in more complexly organized social groups, such as reproductive skew, division of labor, or even nest-sharing. Communal Nesting One step further on the continuum of social behavior is the formation of communal nests. When nesting sites are diffi cult to fi nd ( Michener 1974 ) or construct ( Mccorquodale 1989 ), females may share a single nest, as the costs of nest construction are too high, and successful reproduction may be impossible unless a female joins an established nest ( Neff and Dan- forth 1991 ). In communal nests, individuals reap the benefi ts of mutual nest defense against parasites and aggressive conspecifi cs looking to usurp a nest ( Gamboa 1978 ). But, each female builds, maintains, and provisions only her own section, and cares only for her own young ( Gadau et al. 2009 ; Michener 1974 ). Such nest-sharing can be established when daughters remain at the natal nest and rear their own young, or when multiple females found a nest together. These scenarios have both been argued as possible precursors to eusociality (Lin and Michener 1972). Explicitly, genetic elements (alleles) that bias individuals toward communal living would increase in frequency in populations where communal phenotypes have more offspring on average ( Hölldobler and Wilson 2009 ). Increased fi tness advantages would likely be gained by communal females using fewer resources on nest-founding and because their young would be better protected through communal defense—conferring enhanced female fecundity ( Michener and Lange 1958 ) and offspring survival ( Lin 1964 ). Primitive Eusociality While communal nesters live in social groups together, and sometimes have an overlap in generations, they lack a reproductive division of labor, and do not cooperatively care for THE PATH FROM SOLITARY LIFE TO ADVANCED SOCIAL LIVING 41 their young. To cross the threshold into eusociality, both of these traits must develop. In primitively eusocial insects, there is a reproductive skew in the sense that one individual produces more eggs than the other colony members. These members tend to bias their behavior toward tasks like nest construction, foraging, and raising young cooperatively. Fundamental to primitively eusocial species, though, is that each colony member is still fully capable of reproduction and “queen” and “worker” (helper) castes are not distin- guished by morphology ( Wilson 1971 ). Instead, the queen often maintains her position