The inheritance of alternative nest architectural traditions in stingless bees.

The transmission of complex behavior and culture in humans has long been attributed to advanced forms of social learning,1,2 which play a crucial role in our technological advancement.3 While similar phenomena of behavioral traditions and cultural inheritance have been observed in animals,1,2,4,5,6 including in primates,7 whales,8 birds,9 and even insects,10 the underlying mechanisms enabling the persistence of such animal traditions, particularly in insects, are less well understood. This study introduces pioneering evidence of enduring architectural traditions in the stingless bee Scaptotrigona depilis, which are maintained without any evidence for social learning. We demonstrate that S. depilis exhibits two distinct nest architectures, comprising either helicoidal or flat, stacked horizontal combs, which are transmitted across generations through stigmergy11,12,13,14,15,16,17-an environmental feedback mechanism whereby the presence of the existing comb structures guides subsequent construction behaviors-thereby leading to a form of environmental inheritance.18,19,20 Cross-fostering experiments further show that genetic factors or prior experience does not drive the observed variation in nest architecture. Moreover, the experimental introduction of corkscrew dislocations within the combs prompted helicoidal building, confirming the use of stigmergic building rules. At a theoretical level, we establish that the long-term equilibrium of building in the helicoidal pattern fits with the expectations of a two-state Markov chain model. Overall, our findings provide compelling evidence for the persistence of behavioral traditions in an insect, based on a simple mechanism of environmental inheritance and stigmergic interactions, without requiring any sophisticated learning mechanism, thereby expanding our understanding of how traditions can be maintained in non-human species.

Sex wars: a female genital spine forces male damselflies to shorten copulation duration.

In some species, males use weapons to harm females, increasing their short-term fitness. Here we show that females can use genital adaptations against males. Females of the damselfly Enallagma cyathigerum have a conspicuous vulvar spine on the eighth abdominal segment, which contacts with the male during copulation. We tested 3 hypotheses for its function: it (a) inflicts damage to the male during copulation; (b) facilitates endophytic oviposition; and (c) stimulates males during copulation to increase their investment. We found that males mated on average for 54 min with control females, but increased copulation to 99 min with females without spine. There was no evidence of physical harm of the spine on the male's seminal vesicle, which shows 8- to 18-folds, exactly where the spine contacts during copulation. Females with and without spine exhibited the same egg-laying rates and showed similar fecundity and fertility. Longevity was also similar in males mated to control and spineless females. In contrast to many species where females resist male harassment by behavioral responses, the morphological adaptation observed in E. cyathigerum appears to act as a sexual weapon, allowing females to control copulation duration. We suggest that the spine has evolved because of sexual conflict over mating duration.

Evolution of self-organised division of labour driven by stigmergy in leaf-cutter ants.

Social insects owe their widespread success to their ability to efficiently coordinate behaviour to carry out complex tasks. Several leaf-cutter ant species employ an advanced type of division of labour known as task partitioning, where the task of retrieving leaves is distributed between workers that cut and drop and those that collect the fallen leaves. It is not entirely clear how such highly coordinated behaviour can evolve, as it would seem to require the simultaneous mutations of multiple traits during the same generation. Here, we use an agent-based simulation model to show how task partitioning in leaf-cutter ants can gradually evolve by exploiting stigmergy (indirect coordination through the environment) through gravity (leaves falling from the treetop on the ground forming a cache). Our simple model allows independent variation in two core behavioural dimensions: the tendency to drop leaves and the tendency to pick up dropped leaves. Task partitioning readily evolves even under these minimal assumptions through adaptation to an arboreal environment where traveling up and down the tree is costly. Additionally, we analyse ant movement dynamics to demonstrate how the ants achieve efficient task allocation through task switching and negative feedback control.

Tragedy of the commons in Melipona bees revisited.

Melipona stingless bees display a paradoxical overproduction of queens, which are later eliminated by nest-mate workers. Mechanistically, it was suggested that the monoterpenoid geraniol deposited into newly provisioned cells by adult bees would cause larvae to develop into queens in Melipona beecheii. This system could be evolutionarily stable if many of these new queens were to leave the nest and parasitize other genetically unrelated colonies nearby, as was shown to occur in a congeneric species. Here, we use microsatellite markers to test whether queen overproduction could be a strategy by which adult workers control the caste fate of the developing larvae to export copies of their own genes to the rest of the population via queen parasitism in M. beecheii. In addition, we re-examined whether artificially increasing the levels of geraniol indeed caused larvae to develop as queens rather than workers. Contrary to our prediction, we found no evidence for queen parasitism in M. beecheii and observed no effect of geraniol on the rearing of new queens. Together, these results support the original 'tragedy of the commons' hypothesis for queen overproduction in Melipona bees, where individual larvae selfishly bias their development towards the queen pathway according to their best evolutionary interests.

Zerynthia polyxena Locally Monophagous on Aristolochia pallida in the Susa Valley.

In insect-plant biology, oviposition choices and larval development on different host plants are crucial factors to be investigated. To design conservation strategies for protected Lepidoptera, which are overall oligophagous but locally monophagous, it is important to understand which host plant species is locally preferred. We thus investigated oviposition choices and larval development of the protected butterfly Zerynthia polyxena in controlled laboratory conditions, using three possible host plant species which are present in the Piedmont region: Aristolochia pallida, A. clematitis, and A. rotunda. We found that laboratory conditions are not favorable for Z. polyxena oviposition, even if the fertility of the females was in normal range for Papilionidae. However, we were able to understand the local monophagy of the species on A. pallida in the Susa Valley through larval survival and development stages. Egg hatching was similar among the three host plant species; however, even if larvae eat and grow similarly on the different host plant species until the third larval stage, the only larvae that reached the pupal stage were those fed with A. pallida. In conclusion, whereas Z. polyxena is oligophagous in the rest of Europe for the genus Aristolochia, the species is locally monophagous on A. pallida in the Susa Valley.

Tests of search image and learning in the wild: Insights from sexual conflict in damselflies.

Search image formation, a proximal mechanism to maintain genetic polymorphisms by negative frequency-dependent selection, has rarely been tested under natural conditions. Females of many nonterritorial damselflies resemble either conspecific males or background vegetation. Mate-searching males are assumed to form search images of the majority female type, sexually harassing it at rates higher than expected from its frequency, thus selectively favoring the less common morph. We tested this and how morph coloration and behavior influenced male perception and intersexual encounters by following marked Ischnura elegans and noting their reactions to conspecifics. Contrary to search image formation and associative learning hypotheses, although males encountered the minority, male-like morph more often, sexual harassment and clutch size were similar for both morphs. Prior mating attempts or copula with morphs did not affect a male's subsequent reaction to them; males rarely attempted matings with immature females or males. Females mated early in the day, reducing the opportunity for males to learn their identity beforehand. Once encountered, the male-like morph was more readily noticed by males than the alternative morph, which once noticed was more likely to receive mating attempts. Flexible behavior gave morphs considerable control over their apparency to males, influencing intersexual encounters. Results suggested a more subtle proximal mechanism than male learning maintains these color polymorphisms and call for inferences of learning to be validated by behavior of wild receivers and their signalers.