High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp Polistes canadensis

• Published in: Molecular ecology Vol. 28; no. 13; pp. 3271 - 3284
• Main Authors: Southon, Robin J., Bell, Emily F., Graystock, Peter, Wyatt, Christopher D. R., Radford, Andrew N., Sumner, Seirian
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.07.2019
• Subjects: Animal behavior; Animals; Biological evolution; Ecological monitoring; Eusociality; Evolution; Female; Fitness; Genetic Fitness; Genetic Markers; Genotype; Helping Behavior; Heredity; inclusive fitness; Insects; Life history; Male; Microsatellite Repeats; Microsatellites; Nesting; Nesting Behavior; Nests; Nucleotides; Offspring; Panama; Polistes; Polistes canadensis; Polymorphism; Polymorphism, Single Nucleotide; Queens; relatedness; Reproduction; Reproductive fitness; reproductive skew; Seasonal variations; single nucleotide polymorphisms; Single-nucleotide polymorphism; Social conditions; Tropical environments; Wasps - genetics; Wasps - physiology; Workers (insect caste); Panama; Polistes; relatedness; inclusive fitness; single nucleotide polymorphisms; reproductive skew
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.15137

Explaining the evolution of helping behaviour in the eusocial insects where nonreproductive (“worker”) individuals help raise the offspring of other individuals (“queens”) remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on nontropical species, where seasonality causes family groups to disperse; cofoundresses forming new nests the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here, we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes—Polistes canadensis. Using both microsatellites and newly developed single nucleotide polymorphism markers, we show that adult cofoundresses are highly related and that brood production is monopolized by a single female across the nesting cycle. Nonreproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life history and ecologies when considering the evolution of reproductive strategies.