The inheritance of alternative nest architectural traditions in stingless bees

Viviana Di Pietro,Cristiano Menezes, Maria Giulia de Britto Frediani, David Jos Pereira, Maxime Fajgenblat,Helena Mendes Ferreira,Tom Wenseleers,Ricardo Caliari Oliveira

CURRENT BIOLOGY(2024)

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Abstract
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, 1,2,4-6 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 stigmergy 11-17 -an environmental feedback mechanism whereby the presence of the existing comb structures guides subsequent construction behaviors-thereby leading to a form of environmental inheritance. 18-20 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.
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Key words
animal traditions,environmental inheritance,stigmergy,nest architecture,stingless bees
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