The inheritance of alternative nest architectural traditions in stingless bees

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

doi:10.1016/j.cub.2024.02.073

The inheritance of alternative nest architectural traditions in stingless bees

Curr Biol. 2024 May 6;34(9):1996-2001.e3. doi: 10.1016/j.cub.2024.02.073. Epub 2024 Mar 19.

Authors

Viviana Di Pietro¹, Cristiano Menezes², Maria Giulia de Britto Frediani², David José Pereira², Maxime Fajgenblat³, Helena Mendes Ferreira⁴, Tom Wenseleers⁵, Ricardo Caliari Oliveira⁶

Affiliations

¹ Laboratory of Socioecology and Social Evolution, Department of Biology, KU Leuven, Naamsestraat 59, 3000 Leuven, Belgium. Electronic address: viviana.dipietro@kuleuven.be.
² Embrapa Environment, Laboratory of Entomology and Phytopathology, SP-340 Road, 13918-110 Jaguariúna, Brazil.
³ Laboratory of Freshwater Ecology, Evolution and Conservation, Department of Biology, KU Leuven, Charles Deberiotstraat 32, Leuven 3000, Belgium; I-BioStat, Data Science Institute, Hasselt University, Agoralaan 1, Diepenbeek 3590, Belgium.
⁴ Laboratory of Socioecology and Social Evolution, Department of Biology, KU Leuven, Naamsestraat 59, 3000 Leuven, Belgium.
⁵ Laboratory of Socioecology and Social Evolution, Department of Biology, KU Leuven, Naamsestraat 59, 3000 Leuven, Belgium. Electronic address: tom.wenseleers@kuleuven.be.
⁶ Laboratory of Socioecology and Social Evolution, Department of Biology, KU Leuven, Naamsestraat 59, 3000 Leuven, Belgium; Universitat Autònoma de Barcelona, Departament de Biologia Animal, de Biologia Vegetal i d'Ecologia, Av. de l'Eix Central, edifici C, 08193 Bellaterra (Barcelona), Spain. Electronic address: ricardo.oliveira@uab.cat.

PMID: 38508185
DOI: 10.1016/j.cub.2024.02.073

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^,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.

Keywords: animal traditions; environmental inheritance; nest architecture; stigmergy; stingless bees.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Bees / genetics
Bees / physiology
Nesting Behavior*
Social Behavior
Social Learning