Highlighting the article by Leniaud et al in the November 2015 issue of Insectes Sociaux

Written by Michael Breed, Editor-in-Chief, Insectes Sociaux

In this issue Leniaud et al. (2015) consider the impacts of genes and environment on caste in the silver ant, Cataglyphis bombycina. The topic of genes, environment and caste continues to be a fascinating and complex arena in the study of eusocial insects, and Leniaud et al. present a fascinating contribution to this discussion.

Caste is a fundamental concept in the study of eusocial insects. Differences between the reproductive and the worker caste often extend to morphological specializations that preclude each caste from performing the other’s work. Queens can lack the tools needed for successful foraging but have numerous ovarioles and metabolic capacity to produce large numbers of eggs. Workers of the same species then have reduced or vestigial ovaries, are missing the physical structures needed for mating, and have the morphological tools to allow them to fill the defensive and foraging needs peculiar to their species.

How are such different individuals derived in the course of development? Genes and environment, which are the two major drivers of phenotype, should explain the differences, but what is the relative role of each in caste determination? Thousands of studies of caste determination over the last century have yielded the consensus that caste is largely determined by environment. The precept is that all eggs of the appropriate sex, when laid, are totipotent. This means they have equal potential to yield reproductive or worker adults. When there is more than one worker phenotype then totipotency extends to those differences as well.

But in the last two decades we have come to appreciate that individual response thresholds to tasks can drive worker behavioral choices. These thresholds often reflect genetic differences among workers; this knowledge has brought genetics back into play in conversations about caste and task performance in eusocial insects.

Leniaud et al. take on a much different, but equally exciting, aspect of the overall question of gene/environment interactions in caste in eusocial insects. In Cataglyphis bombycina there are two distinct worker castes. One of these fits the norm for most ants—workers which are, within the caste, morphologically uniform but variable in size. This size variance is associated with task performance.

The other worker caste in Cataglyphis bombycina, though, is unusual. Soldiers are relatively invariant in size and stand as a morphologically distinct group from the workers. This contrasts with many ants in which “soldiers” are workers from the large end of the size spectrum. Soldier distinctiveness as a caste is also known in some types of termites and a few other ant species.

Leniaud et al (2015) found that environment likely is the preponderant influence on caste determination in Cataglyphis bombycina. This fits well with the consensus model of totipotency. In a few colonies, though, they found evidence for a genetic influence on soldier determination based on patrilineal effects. These results are highly important because they suggest that if we backtrack in our thinking about gene X environment interactions in caste determination we may find other examples in which genetic influences, while smaller than environmental influences, are nonetheless present and important in the development of workers during caste differentiation. The results in this paper are well worth considering in the continuing search for the mechanisms of caste differentiation.

Leniaud L, Pearcy M, Taheri A, Aron S (2015) Testing the genetic determination of the soldier caste in the silver ant. Ins. Soc. 62:517-524

The editors of Insectes Sociaux wish to thank, on the behalf of the IUSSI community, these individuals who volunteered their time and effort in reviewing submissions for Volume 62 of the journal.

Xavier Arnan, BT Barton, Grzesiek Buczkowski, Ana Maria Bonetti, Martin Bollazzi, Thomas Bourguignon, Nadine Chapman, Alessandro Cini, Chelsea Cook, Michel Chapuisat, Felipe Contrera, Roberto S. Camargo, Robin M. Crewe, Rita Cervo, Rebecca Maria Clark, Siliva Claver, Tomer Czaczkes, Mary L. Cornelius, MA Costa, Paulo Silvio Damisio da Silva, Francesca Dani, Jacques Delabie, Kleber Del-Claro, Marco Antonio Del Lama, Jean-Marc Devaud, Henry Disney, Heike Feldhaar, Luis Flores-Prado, Vincent Fourcassie, Denis Fournier, Raghavendra Gadagkar, Tugrul Giray, Michael A.D. Goodisman, Michael Greene, Eleanor Groden, Irena M. Grzes, Christopher Hamm, Rob Hammond, Robert Hanus,   Juergen Heinze, John Heraty, Shingo Hosoishi, Kenneth Howard, Michael Hrncir, William O.H. Hughes, Claudia Husseneder, Stefan Jarau, Christian Jost, Timothy Judd, Karen M. Kapheim, Mike Kaspari, Stefanie Kautz, Scott Kight, Sarah Kocher, Suzanne Koptur, Daniel Kronauer, Lori Lach, Jean-Paul Lachaud, Edward LeBrun, Phil Lester, Vernard R. Lewis, Elinor Lichtenberg, Juergen Liebig, Pedro A.C. Lima Pequeno, Kevin Loope, Maria Cristina Lorenzi, Piotr Lukasik, Salima Machkour M’Rabet, Bram Mabelis, Scott MacIvor, William Mackay, Jonathan Majer, Mirian D. Marques, Katie Marshall, Stephen Martin, Kenji Matsuura, William May-Itza, Helen McCreery, Terry McGlynn, Jannette D. Mitchell, Slawomir Mitrus, Toru Miura, Thibaud Monnin, Floria Mora-Kepfer, Corrie Moreau, Nilson Nagamoto, Anjan Nandi, Kristine Nemec, Kok-Boon Neoh, James C Nieh, Elina Nino, Fernando B. Noll, Victoria Norman, Elise Nowbahari, Sean O’Donnell, John Noyes Joachim Offenberg, Laurence Packer, Christian Peeters, Alice Pinto, Christian Pirk, Carlo Polidori, Sanford D. Porter, Michael Poulsen, Scott Powell, J Javier G Quezada-Euan, Yves Quinet, Christian Rabeling, Nigel Raine, Julian Resasco, Freddie-Jeanne Richard, Simon K. Robson, Lesley Rogers, Daniela Romer, Virginie Roy, Jacob A. Russell, Nathan J. Sanders, Jailson Santos de Novais, Amy Savage, Ricarda Scheiner, Ellen Schluns, Thomas Seeley, Bernhard Seifert, Shafir Sharoni, Michael Sheehan, Matthew Siderhurst, Lisa Signorotti, Rabern Simmons, Adam Smith, Philip Starks, Andy Suarez, Liselotte Sundstrom, Allen Szalanski, Timothy Szewczyk, Elizabeth A. Tibbetts, Simon M. Tierney, Etienne Toffin, Juliana Toledo Lima, James Trager, Koji Tsuchida, Neil Tsutsui, Scott Turner, Elodie Urlacher, Maryse Vanderplanck, Edward L. Vargo, Favio Gerardo Vossler, Phil Ward, Natapot Warrit, Michael Weiser, James K. Wetterer, Diana E. Wheeler, Erin Wilson-Rankin, Maureen S. Wright, Aya Yanagawa, Tsuyoshi Yoshimura

Miriam Richards, Associate Editor, Insectes Sociaux

In a recent issue of Insectes Sociaux, we described a rather surprising example of behavioural flexibility in an obligately eusocial sweat bee, Halictus ligatus (Rehan et al. 2013). This is a particularly well studied species that has been the subject of hundreds and hundreds of hours of behavioural observations. As in many eusocial sweat bees, there is considerable evidence in H. ligatus for queen-worker conflict over oviposition rights in Brood 2, a conflict that often results in queen domination, if not monopolization, of Brood 2 egg-laying. Many H. ligatus queens appear to be multiply mated, so relatedness of workers to queen-produced brood is low enough to suggest that workers might often achieve higher fitness through personal reproduction rather than by raising siblings (Richards et al. 1995). Why don’t workers that are bullied by queens and which can’t lay eggs in the natal nest simply leave and raise their own brood somewhere? The lack of any evidence that H. ligatus workers ever start their own nests suggested that they were not capable of doing so, although the reasons why not remained mysterious.[1]

We now know that H. ligatus workers can found their own nests, but only under very specific circumstances (Rehan et al. 2013). This was an unexpected discovery during the course of a summer’s fieldwork on several species of social sweat bees nesting in a huge dirt pile created in the course of university landscaping activities. Knowing the dirt pile was likely to be disturbed again as soil was added and removed by the gardeners, we observed and excavated sweat bee nests throughout the summer. In early July, around the time that workers first emerge from their nests to provision Brood 2, little black wasps in the genus Astata, suddenly began nesting activities right amongst the H. ligatus nests. Their digging activities so severely disrupted sweat bee burrows that newly emerged workers returning from their first foraging trips were unable to find relocate their nests. Some of these workers responded to the loss of their natal burrows by founding new burrows. In so doing, their behaviour perfectly recapitulated the behaviour of spring foundresses – they dug tunnels, excavated brood cells, then provisioned them and laid eggs. In a separate paper, we also discovered evidence for queen renesting in the face of the wasp disruptions: one or two nests appeared to have been so damaged by the wasps, that the queens lost contact with their workers and were forced to provision Brood 2 themselves (Richards et al. 2015). Years ago, I saw the same thing happen when H. ligatus queens nesting in excessively wet soil lost their worker broods to rot.

So, these observations demonstrate that H. ligatus workers can found their own nests and raise their own brood, and yet, they only do so in response to complete loss of contact with their natal nests and nestmates. That workers can establish their own nests reinforces the conclusion that workers are totipotent, potentially capable of expressing both normal worker behaviour and behaviour more typical of queens. On the other hand, it suggests that there are limits to behavioural flexibility, as mid-summer nest-founding would seem to be possible only in response to orphaning, but not as a means of evading aggression and manipulation by queens. Similarly, queens only forage in mid-summer if none of their workers survive to adulthood – the emergence of even a single worker results in queen behaviour by the foundress (sometimes with the result that the queen works her single helper to death in a very short time).

Halictus ligatus is not the only eusocial sweat bee in which nests are founded in mid-summer, but the phenomenon seems to be quite rare. To date, only in one study of Lasioglossum baleicum, has there been a comparison of rates of brood production in spring vs, summer-founded nests. As it turns out, workers that founded their own nests and raised brood solitarily had lower inclusive fitness than those that remained as helpers in the natal nest (Yagi and Hasegawa 2012). However, the high frequency of worker nest-founding in the L. baleicum study suggests that even if worker altruism in the natal nest is a better strategy for workers than founding their own nests, the latter could still be adaptive as a conditional response environmental insult that deprives workers of opportunities to increase inclusive fitness through helping.

Mid-summer nest-founding in H. ligatus and other social species reflects a previously unappreciated ability of female sweat bees to renest in the face of devastating and unpredictable damage to their nests. With the advantage of hindsight, perhaps renesting ability should not be surprising – sweat bees are well known for their preference for nesting in disturbed habitats where their nests are likely often to be trampled by animals or damaged by rain or erosion. In fact, the nesting aggregation where we did this work was colonized soon after the soil was dumped and lasted only a few years until grass and thistles covered the ground, discouraging bees from establishing new nests. Perhaps our surprise just reflects the fact that even those of us who spend a lot of time with these interesting little bees tend to under-estimate their ability to adapt to an unpredictable environment.

[1] Indeed, this question was asked repeatedly at my PhD defense by an eminent insect physiologist who was apparently quite irritated by my suggestion that sweat bee queens aggressively force workers to remain in the natal nest as helpers, preventing them from laying their own eggs. He asked rather pointedly (and repeatedly) why the bullied workers didn’t just leave the nest. Eventually, the social psychologist on the examining committee got quite annoyed and pointed out the similarity between bullied workers and abused women who also don’t leave aggressive spouses – not to mention the similar attitudes of onlookers who wonder why the women don’t just leave.   The argument between my examiners continued to escalate until George Eickwort, also an eminent entomologist and expert on social sweat bees, intervened and agreed with me. The eminent physiologist remained highly skeptical (and rather grumpy), but at least my thesis defense was not completely derailed!

Highlighting an article in the current issue of Insectes Sociaux:
Charbonneau D, Hillis N, Dornhaus A. ‘Lazy’ in nature: ant colony time budgets show high ‘inactivity’ in the field as well as in the lab. Insectes Sociaux 62. doi: 10.1007/s00040-014-0370-6

Does the highly touted efficiency of social insect colonies stem from a dedicated work force? Are all animals in the society engaged at the highest possible level in their work? Intuition and fairy tales, such as Aesop’s fable of the ant and the grasshopper, tell us this is exactly the case. But even casual observation of a social insect colony reveals the puzzling truth: many workers are inactive at any given moment and rarely, if ever, does the entire colony stir into concerted action. This observation of lazy workers or helpers extends to vertebrate societies including the euso- cial naked mole rat [6]. An animal society, including a social insect colony, can appear to be the exact opposite of the paragon of efficiency.

A number of hypotheses attempt to explain this observation. The first invokes workers held in reserve for rare but essential tasks [4]. This has also been expressed as the concept that workers or helpers may be in a holding pattern waiting to fill in as needed [1]. Second, worker ineffectiveness is possible due to genetic variation in worker response thresholds not matching the distribution of tasks at hand [2]. Third, Mattila et al. [5] put forward the intriguing idea that workers in colonies monogamous queens focus more on reproductive competition and less on work than workers in polygynous colonies, meaning that workers’ activities in monogamous colonies are more biased to reproduction rather than labor.

In an interesting article in this issue, Charbonneau and colleagues [3] note that most of the observations of lazy workers in eusocial insect colonies have been obtained from laboratory colonies. This brings into question the validity of the lazy worker concept as differences in the demand for work in the laboratory, as compared to field settings, may create behavioral artifacts in division of labor among workers. Charbonneau and colleagues compare the behavior of workers in laboratory and field colonies of Temnothorax rugulatus, a species of ant commonly used for laboratory studies.

Their key finding is that division of labor in the laboratory colonies closely matches that of field colonies. While this could seem like a simple confirmation of the soundness of previously published laboratory studies, the significance of this work has far reaching implications for our understanding of division of labor. Even rate of foraging behavior, for which labor demands could be quite different between laboratory and field colonies, showed no significant differences in time budget between the two settings.

The reason for the presence of lazy workers remains to be discovered. Of particular interest will be the determination of whether a single underlying explanation covers all cases. If so, this could reflect fundamental algorithms that govern division of labor. On the other hand, the widespread presence of lazy workers may reflect convergence on a behavioral phenotype with many possible roots. The reserve force/holding pattern explanation seems most generally plausible based on the slender evidence available. Future studies on how task performance is replaced when workers are removed should help to sort this out. In the meantime, we can be sure that social insect workers are not governed by the moral drive to work asserted in Aesop’s fable.

Michael Breed Editor-in-Chief

References
1. Baglione V., Canestrari D., Chiarati, E., Vera R. and Marcos J. M. 2010. Lazy group members are substitute helpers in carrion crows. Proc. Roy. Soc. B-Biol. Sci. 277: 3275-3282.
2. Bonabeau E., Theraulaz G. and Deneubourg J.-L. 1998. Fixed Response thresholds and the regulation of division of labor in insect societies. Bull. Mathemat. Biol. 60: 753–807.
3. Charbonneau D, Hillis N, Dornhaus A. ‘Lazy’ in nature: ant colony time budgets show high ‘inactivity’ in the field as well as in the lab. Insectes Sociaux 62. doi: 10.1007/s00040-014-0370-6
4. Jandt J. M., Robins N. S., Moore R. E. and Dornhaus A. 2012. Individual bumblebees vary in response to disturbance: a test of the defensive reserve hypothesis. Insect. Soc. 59: 313–321.
5. Mattila H. R., Reeve H. K. and Smith M. L. 2012. Promiscuous honey bee queens increase colony productivity by suppressing worker selfishness. Curr. Biol. 22: 2027–2031.
6. Reeve H. K. 1992 Queen activation of lazy workers in colonies of the eusocial naked molerat. Nature 358: 147–149.

Published online: 8 January 2015
 in Insectes Sociaux
Copyright International Union for the Study of Social Insects (IUSSI) 2015