scholarly journals What Can Mechanisms Underlying Derived Traits Tell Us About the Evolution of Social Behavior?

Author(s):  
Erin Treanore ◽  
Nathan Derstine ◽  
Etya Amsalem

Abstract Social behavior, although rare, is a highly successful form of living that has reached its most extreme forms in eusocial insects. A tractable framework to understand social evolution is the study of major transitions in social behavior. This includes the transitions between solitary to social living, from species exhibiting intermediate degrees of sociality to species exhibiting true sociality, and from primitive to advanced eusocial species. The latter transition is characterized by the emergence of traits not previously found in primitive eusocial species, such as fixed morphological differences between castes and task specialization within the sterile caste. Such derived traits appear to exist in a binary fashion, present in advanced eusocial species, and absent or rare in primitive ones, and thus do not exist in a gradient that is easily tracked and compared between species. Thus, they may not be viewed as valuable to explore ultimate questions related to social evolution. Here, we argue that derived traits can provide useful insights on social evolution even if they are absent or rare in species with a lower social organization. This applies only if the mechanism underlying the trait, rather than the function it regulates for, can be traced back to the solitary ancestors. We discuss two examples of derived traits, morphological differences in female castes and primer pheromones regulating female reproduction, demonstrating how their underlying mechanisms can be used to understand major transitions in the evolution of social behavior and emphasize the importance of studying mechanistic, rather than functional continuity of traits.

Author(s):  
Heikki Helanterä

If the logic of natural selection is applied strictly at the level of individual production of offspring, sterile workers in insect societies are enigmatic. How can natural selection ever produce individuals that refrain from reproduction, and how are traits of such individuals that never produce offspring scrutinized and changed through natural selection? The solution to both questions is found in the family structures of insect societies. That is, the sterile helper individuals are evolutionary altruists that give up their own reproduction and instead are helping their kin reproduce and proliferate shared genes in the offspring of the fertile queen. Selection in such cases is not just a matter of individual’s direct reproduction, and instead of own offspring, the currency of the evolutionary success of sterile individuals is inclusive fitness. The concept of inclusive fitness and the process of kin selection are key to understanding the magnificent cooperation we see in insect societies, and reciprocally, insect societies are key case studies of inclusive fitness logic. In extreme cases, such as the highly advanced and sophisticated societies of ants, honeybees, and termites, the division of labor and interdependence of colony members is so complete, that it is justified to talk about a new level of evolutionary individuality. Such increases in the hierarchical complexity of life are called major transitions in evolution. We see adaptations of the colony, rather than individuals, in, e.g., their communication and group behaviors. The division of labor between morphologically differentiated queens and workers is analogous to germline-soma separation of a multicellular organism, justifying the term superorganism for the extreme cases of social lifestyle. Alongside these extreme cases, there is enormous diversity in the social lifestyles across social insect taxa, which provides a window into the balance of cooperation and conflict, and individual reproduction and helping others, in social evolution. Over the last decades, social insect research has been an area where the theoretical and empirical understanding have been developed hand in hand, together with examples of wonderful natural history, and has tremendously improved our understanding of evolution.


Author(s):  
Ysabel Milton Giraldo ◽  
Mario L. Muscedere ◽  
James F. A. Traniello

Are eusociality and extraordinary aging polyphenisms evolutionarily coupled? The remarkable disparity in longevity between social insect queens and sterile workers—decades vs. months, respectively—has long been recognized. In mammals, the lifespan of eusocial naked mole rats is extremely long—roughly 10 times greater than that of mice. Is this robustness to senescence associated with social evolution and shared mechanisms of developmental timing, neuroprotection, antioxidant defenses, and neurophysiology? Focusing on brain senescence, we examine correlates and consequences of aging across two divergent eusocial clades and how they differ from solitary taxa. Chronological age and physiological indicators of neural deterioration, including DNA damage or cell death, appear to be decoupled in eusocial insects. In some species, brain cell death does not increase with worker age and DNA damage occurs at similar rates between queens and workers. In comparison, naked mole rats exhibit characteristics of neonatal mice such as protracted development that may offer protection from aging and environmental stressors. Antioxidant defenses appear to be regulated differently across taxa, suggesting independent adaptations to life history and environment. Eusocial insects and naked mole rats appear to have evolved different mechanisms that lead to similar senescence-resistant phenotypes. Careful selection of comparison taxa and further exploration of the role of metabolism in aging can reveal mechanisms that preserve brain functionality and physiological resilience in eusocial species.


Author(s):  
Iris Steitz ◽  
Robert J Paxton ◽  
Stefan Schulz ◽  
Manfred Ayasse

AbstractIn eusocial insects, chemical communication is crucial for mediating many aspects of social activities, especially the regulation of reproduction. Though queen signals are known to decrease ovarian activation of workers in highly eusocial species, little is known about their evolution. In contrast, some primitively eusocial species are thought to control worker reproduction through physical aggression by the queen rather than via pheromones, suggesting the evolutionary establishment of chemical signals with more derived sociality. However, studies supporting this hypothesis are largely missing. Socially polymorphic halictid bees, such as Halictus rubicundus, with social and solitary populations in both Europe and North America, offer excellent opportunities to illuminate the evolution of caste-specific signals. Here we compared the chemical profiles of social and solitary populations from both continents and tested whether (i) population or social level affect chemical dissimilarity and whether (ii) caste-specific patterns reflect a conserved queen signal. Our results demonstrate unique odor profiles of European and North American populations, mainly due to different isomers of n-alkenes and macrocyclic lactones; chemical differences may be indicative of phylogeographic drift in odor profiles. We also found common compounds overproduced in queens compared to workers in both populations, indicating a potential conserved queen signal. However, North American populations have a lower caste-specific chemical dissimilarity than European populations which raises the question if both use different mechanisms of regulating reproductive division of labor. Therefore, our study gives new insights into the evolution of eusocial behavior and the role of chemical communication in the inhibition of reproduction.


2015 ◽  
Vol 282 (1811) ◽  
pp. 20150704 ◽  
Author(s):  
J. Frances Kamhi ◽  
Kelley Nunn ◽  
Simon K. A. Robson ◽  
James F. A. Traniello

Complex social structure in eusocial insects can involve worker morphological and behavioural differentiation. Neuroanatomical variation may underscore worker division of labour, but the regulatory mechanisms of size-based task specialization in polymorphic species are unknown. The Australian weaver ant, Oecophylla smaragdina , exhibits worker polyphenism: larger major workers aggressively defend arboreal territories, whereas smaller minors nurse brood. Here, we demonstrate that octopamine (OA) modulates worker size-related aggression in O. smaragdina . We found that the brains of majors had significantly higher titres of OA than those of minors and that OA was positively and specifically correlated with the frequency of aggressive responses to non-nestmates, a key component of territorial defence. Pharmacological manipulations that effectively switched OA action in major and minor worker brains reversed levels of aggression characteristic of each worker size class. Results suggest that altering OA action is sufficient to produce differences in aggression characteristic of size-related social roles. Neuromodulators therefore may generate variation in responsiveness to task-related stimuli associated with worker size differentiation and collateral behavioural specializations, a significant component of division of labour in complex social systems.


2019 ◽  
Vol 6 (8) ◽  
pp. 190283
Author(s):  
Teppei Jono ◽  
Yosuke Kojima ◽  
Takafumi Mizuno

Eusocial insects can express surprisingly complex cooperative defence of the colony. Brood and reproductive castes typically remain in the nest and are protected by workers' various antipredator tactics against intruders. In Madagascar, a myrmicine ant, Aphaenogaster swammerdami , occurs sympatrically with a large blindsnake, Madatyphlops decorsei . As blindsnakes generally specialize on feeding on termites and ants brood by intruding into the nest, these snakes are presumably a serious predator on the ant. Conversely, a lamprophiid snake, Madagascarophis colubrinus , is considered to occur often in active A . swammerdami nests without being attacked. By presenting M . colubrinus , M . decorsei and a control snake, Thamnosophis lateralis , at the entrance of the nest, we observed two highly specialized interactions between ants and snakes: the acceptance of M . colubrinus into the nest and the cooperative evacuation of the brood from the nest for protection against the ant-eating M . decorsei . Given that M . colubrinus is one of the few known predators of blindsnakes in this area, A . swammerdami may protect their colonies against this blindsnake by two antipredator tactics, symbiosis with M . colubrinus and evacuation in response to intrusion by blindsnakes. These findings demonstrate that specialized predators can drive evolution of complex cooperative defence in eusocial species.


2017 ◽  
Vol 114 (25) ◽  
pp. 6569-6574 ◽  
Author(s):  
Bernadette Wittwer ◽  
Abraham Hefetz ◽  
Tovit Simon ◽  
Li E. K. Murphy ◽  
Mark A. Elgar ◽  
...  

Social animals must communicate to define group membership and coordinate social organization. For social insects, communication is predominantly mediated through chemical signals, and as social complexity increases, so does the requirement for a greater diversity of signals. This relationship is particularly true for advanced eusocial insects, including ants, bees, and wasps, whose chemical communication systems have been well-characterized. However, we know surprisingly little about how these communication systems evolve during the transition between solitary and group living. Here, we demonstrate that the sensory systems associated with signal perception are evolutionarily labile. In particular, we show that differences in signal production and perception are tightly associated with changes in social behavior in halictid bees. Our results suggest that social species require a greater investment in communication than their solitary counterparts and that species that have reverted from eusociality to solitary living have repeatedly reduced investment in these potentially costly sensory perception systems.


2021 ◽  
Vol 9 ◽  
Author(s):  
Ken Sasaki ◽  
Yasukazu Okada ◽  
Hiroyuki Shimoji ◽  
Hitoshi Aonuma ◽  
Toru Miura ◽  
...  

Convergent evolution of eusociality with the division of reproduction and its plastic transition in Hymenoptera has long attracted the attention of researchers. To explain the evolutionary scenario of the reproductive division of labor, several hypotheses had been proposed. Among these, we focus on the most basic concepts, i.e., the ovarian ground plan hypothesis (OGPH) and the split-function hypothesis (SFH). The OGPH assumes the physiological decoupling of ovarian cycles and behavior into reproductive and non-reproductive individuals, whereas the SFH assumes that the ancestral reproductive function of juvenile hormone (JH) became split into a dual function. Here, we review recent progress in the understanding of the neurohormonal regulation of reproduction and social behavior in eusocial hymenopterans, with an emphasis on biogenic amines. Biogenic amines are key substances involved in the switching of reproductive physiology and modulation of social behaviors. Dopamine has a pivotal role in the formation of reproductive skew irrespective of the social system, whereas octopamine and serotonin contribute largely to non-reproductive social behaviors. These decoupling roles of biogenic amines are seen in the life cycle of a single female in a solitary species, supporting OGPH. JH promotes reproduction with dopamine function in primitively eusocial species, whereas it regulates non-reproductive social behaviors with octopamine function in advanced eusocial species. The signal transduction networks between JH and the biogenic amines have been rewired in advanced eusocial species, which could regulate reproduction in response to various social stimuli independently of JH action.


2019 ◽  
Vol 74 (9-10) ◽  
pp. 221-231 ◽  
Author(s):  
Abraham Hefetz

Abstract Primer pheromones play a pivotal role in the biology and social organization of insect societies. Despite their importance, they have been less studied because of the complexity of the required bioassays and, consequently, only a few of them have been chemically identified to date. The major primer pheromones are that of the queen pheromones that regulate reproductive skew and maintain colony cohesion and function. From a theoretical viewpoint, several features regarding the chemistry of queen pheromones can be predicted. They should be generally nonvolatile in order to avoid saturation of the colony space, which might otherwise hamper their perception because of sensory habituation. Accordingly, they should be actively dispersed throughout the colony by workers. The queen pheromone should also be caste-specific, qualitatively different from any worker pheromone, and preferably multicomponent, to allow unequivocal identification of the queen. The bi-potency of the female larvae in social Hymenoptera to become queen or worker necessitates strict regulation over pheromone production. Indeed, in the honeybee, the biosynthetic pathways as well as the genomic expressions are completely disparate between queens and workers. Future advances in chemical analyses, transcriptomics, proteomics, and metabolomics will enrich our understanding of the chemistry, mechanisms, and crucial role that primer pheromones play in social evolution.


2019 ◽  
Vol 286 (1916) ◽  
pp. 20191815 ◽  
Author(s):  
Wyatt A. Shell ◽  
Sandra M. Rehan

The evolutionary origins of advanced eusociality, one of the most complex forms of phenotypic plasticity in nature, have long been a focus within the field of sociobiology. Although eusocial insects are known to have evolved from solitary ancestors, sociogenomic research among incipiently social taxa has only recently provided empirical evidence supporting theories that modular regulation and deeply conserved genes may play important roles in both the evolutionary emergence and elaboration of insect sociality. There remains, however, a paucity of data to further test the biological reality of these and other evolutionary theories among taxa in the earliest stages of social evolution. Here, we present brain transcriptomic data from the incipiently social small carpenter bee, Ceratina calcarata , which captures patterns of cis -regulation and gene expression associated with female maturation, and underlying two well-defined behavioural states, foraging and guarding, concurrently demonstrated by mothers and daughters during early autumn. We find that an incipiently social nest environment may dramatically affect gene expression. We further reveal foraging and guarding behaviours to be putatively caste-antecedent states in C. calcarata , and offer strong empirical support for the operation of modular regulation, involving deeply conserved and differentially expressed genes in the expression of early social forms.


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