Neotropical wasps were ruled by workers some 55 million years ago

A study by researchers at São Paulo State University reinforces the idea that environmental and climate-related changes resulting from the Andean uplift triggered a revolution in the caste system of these paper wasps.

By André Julião  |  Agência FAPESP – The uplift of the Andes between 54 million and 57 million years ago caused a number of environmental and climate-related changes that revolutionized the wasp world. A caste system in which only one queen laid eggs while sterile workers performed all other tasks in the colony gave way to a system with more reproductive parity. Several females could now be fertile, but a new caste punished queens that laid fewer eggs by cutting off their wings and evicting them from the colony. At the same time, nests were protected externally against ants, the main enemy of wasps. The upshot was the emergence of the tribe Epiponini, paper wasps known in Brazil as marimbondos or cabas.

The conclusion is part of the findings of a broad study published in the journal Cladistics. The authors are researchers at São Paulo State University (UNESP) and the University of São Paulo (USP) in Brazil, and at the American Museum of Natural History and the Carnegie Museum of Natural History in the United States.

“In addition to the difference in castes, Epiponini stand out for the significant diversity of their nest architecture. Practically every genus has nests with a distinctive shape. In this phylogenetic study, we found that their common ancestor apparently already built what we scientists call an envelope – an enclosure that probably became an evolutionary advantage because it shielded the nest from enemies, especially ants,” Fernando Noll, principal investigator for the study, told Agência FAPESP. Noll is a professor at UNESP’s Institute of Biosciences, Letters and Exact Sciences (IBILCE) in São José do Rio Preto.

The study was funded by FAPESP as part of the project “Molecular phylogeny of Epiponini and the relationships among basal genera (Hymenoptera, Vespidae)”.

“A well-established phylogeny is vital to an understanding of a group’s evolutionary scenarios. In the last 20 years, the prevalent phylogeny has become incompatible with a number of observations made about these paper wasps,” Noll said. 

Phylogenies can be thought of as evolutionary hypotheses that describe kinships among living beings. The study in question focused on the subfamily Polistinae, and especially the tribe Epiponini, which is endemic to the Neotropics (from Texas to northern Argentina) and quite diverse, comprising some 250 species in 19 genera. Epiponini belongs to the family Vespidae, which in turn belongs – with bees (Apoidea), ants (Apocrita) and other insects generically classed as wasps – to the order Hymenoptera.

Dictatorship of the proletariat

The word marimbondo comes from Kimbundu, a language spoken in Angola, and was used by the Portuguese to refer pejoratively to Brazilians during the colonial period around the time of Brazil’s declaration of independence. In northern Brazil, the insect is called caba, a word that comes from Tupi, an Amerindian language.

To Brazilians, these wasps are legendary for their aggressiveness and the shape and size of their nests. Their vernacular names include marimbondo-sargento (Polybia liliaceae and P. jurinei), which has a sergeant’s stripes on its thorax; vespa-tatu (Synoeca surinama), whose nest envelope recalls the shell of an armadillo; marimbondo-chapéu (genus Apoica), whose nest resembles a hat; and marimbondo-prateleira (Agelaia vicina), whose multilayered nest recalls a set of shelves. 

For the study, the researchers collected specimens from several parts of Brazil and borrowed some from other institutions’ collections. The specimens analyzed belonged to a total of 143 species representing all tribes of the subfamily Polistinae, as well as other wasps for comparison.

DNA samples were taken from the specimens, and the researchers then amplified COI, a gene used for species identification, and others relating to morphology and nest-building behavior. Computational tools joined up the data to produce a description of the subfamily and pinpoint the evolutionary position of each tribe and genus.

“When most people think of social insects, the one that comes to mind is usually the European honeybee, Apis mellifera, where there’s a single queen with significant reproductive potential and distinctive morphology. Submitted to the queen, a caste of sterile workers perform tasks such as brood care and foraging. In Epiponini, we found that evolution led to the reverse of this setup. At some point, they ceased to have a single queen and many females became fertile in the same colony. Later on, some lineages reacquired this trait,” Noll said.

The study also showed that the common ancestor of Epiponini developed a violent method for selecting the most fertile members of a colony, still present now in most species. Some 55 million years ago, the so-called intolerant female – a queen that violently eliminated other fertile females – was replaced by several tolerant (or totipotent) females that allowed more than one individual to be fertile and lay eggs. This was an evolutionary advantage for the group because it assured survival of the colony while swarming, when all or some wasps leave the nest to form new colonies. Relations remained violent, however, owing to the emergence of another caste that aggressively punished less productive queens.

“They’re a reproductive police force,” Noll said. “Queens that produce fewer eggs have their wings cut off and are evicted from the nest. There’s even a ritual dance. Queens that don’t perform it correctly are eliminated by the workers. When a nest is started, there are several reproductive females, but over time the number dwindles until only the most productive individuals remain. This drastic change in their society has permitted the considerable diversification we see now.” As with other social insects, males are removed from the colony or die naturally after mating.

The article “Marimbondos: systematics, biogeography, and evolution of social behavior of Neotropical swarm-founding wasps (Hymenoptera: Vespidae: Epiponini)” is at: onlinelibrary.wiley.com/doi/abs/10.1111/cla.12446.