Distributed physiology and the molecular basis of social life in eusocial insects

Abstract

The traditional focus of physiological and functional genomic research is on molecular processes that play out within a single body. In contrast, when social interactions occur, molecular and behavioral responses in interacting individuals can lead to physiological processes that are distributed across multiple individuals. In eusocial insect colonies, such multi-body processes are tightly integrated, involving social communication mechanisms that regulate the physiology of colony members. As a result, conserved physiological mechanisms, for example related to pheromone detection and neural signaling pathways, are deployed in novel contexts and regulate emergent colony traits during the evolutionary origin and elaboration of social complexity. Here we review conceptual frameworks for organismal and colony physiology, and highlight functional genomic, physiological, and behavioral research exploring how colony-level traits arise from physical and chemical interactions among nestmates. We highlight mechanistic work exploring how colony traits arise from physical and chemical interactions among physiologically-specialized nestmates of 1 various developmental stages. We consider similarities and differences between organismal and colony physiology, and make specific predictions based on a decentralized perspective on the function and evolution of colony traits. Integrated models of colony physiological function will be useful to address fundamental questions related to the evolution and ecology of collective behavior in natural systems. Colony Organization = Social Anatomy + Social PhysiologyEusocial colonial insects, such as ants, termites, and honey bees, thrive across almost all terrestrial ecosystems 1,2 . The ecological success of these species rests in their use of colony traits, such as nest architecture 3,4 and collective foraging behavior 5-7 , which are functionally absent in solitary insects yet keenly developed in eusocial taxa. In the eusocial insects, division of labor (DOL) describes how nestmates vary in their form and function. DOL formalizes the extent of specialization among nestmates in the performance of tasks, usually with a physiological or morphological basis or arising from nestmate age (temporal polyethism) and experience [8][9][10][11] . We build off of the conceptual framework of Johnson & Linksvayer 12 that considers eusocial colony organization from the perspective of social anatomy & social physiology : Social anatomy is the notion that colonies are composed of specialized parts with limited roles, like the organs of an individual animal. Specialized colony anatomy allows for greater productivity and efficiency for the completion of many tasks.Physiological specialization exists at multiple levels within the colony. Queen-worker specialization allows for an increased reproductive output of queens alongside increased work output from workers, from the same diploid female genome 13 .Subspecialization among workers can manifest as permanent variation in body morphology 14 , temporal polyet...

Eusociality and the evolution of aging in superorganisms

“…Besides different levels of relatedness, complex eusocial societies can be compared to simple multicellular organisms. Recently it has been suggested that social anatomy, referring to colonies being composed of specialized individuals, and social physiology, the set of mechanisms that coordinate the activity and the development of specialized individuals, (Friedmann et al 2020) parallel anatomy and physiology of multicellular organisms. Thus, the study of caste-specific aging and its underlying mechanisms may shed light on the evolution of aging patterns in early metazoans and on tissue-specific aging in advanced metazoans such as ourselves.…”

Collective Regulation of Metabolism, Development and Longevity Through a Socially Exchanged Fluid

“…While most previous work has focused almost exclusively on gene expression, this research shows that for species that engage in trophallaxis, expression studies are necessary but insufficient to understand where in the colony the relevant genes are having their effects. It is conceivable that proteins produced in certain individuals could be sequestered by other individuals, allowing transmission of critical materials across superorganismal tissues (Friedman et al, 2020). In this view, proteins that exert effects in different individuals than the individuals that have produced them can be considered superorganismal hormones.…”

Genetics of Social Behavior

“…As a result of the web of social interactions and social interdependency of individuals within social insect colonies, the molecular mechanisms underlying the expression of social behaviorand other traitsin social insect colonies are likely much more complex, involving genes and pathways distributed across multiple interacting individuals, when compared to the traits of solitary organisms that are at least less influenced by interactions with conspecifics [4,13]. Furthermore, genetic variation in the genomes of both the individual expressing the trait and her/his social partners (i.e., through direct or indirect genetic effects, respectively) may contribute to trait variation for individual-level traits, as well as for colony-level traits.…”