Mixed modes of reproduction, combining sexual processes with thelytokous parthenogenesis, occur in all major clades of social insects. In several species of termites, queens maximize their genetic input into nondispersing replacement queens through parthenogenesis, while maintaining genetically diverse sterile offspring and dispersing reproductives via sexual reproduction. This so-called asexual queen succession (AQS) has multiple independent origins and its presumed advantages are diverse as well, ranging from multiplication of colony reproductive potential to extension of its lifespan beyond that of the foundress. However, how AQS shapes colony life cycles under natural conditions remains poorly known. The neotropical termite Silvestritermes minutus inhabits small but conspicuous nests, offering a unique opportunity to investigate the impact of AQS on life history. We report on its breeding system, life cycle and sex allocation using social structure census in 137 nests and genotyping of 12 colonies at 12 microsatellite loci. We show that colonies are established by an outbred pair of primary reproductives. In less than 2 years, the foundress is replaced by multiple neotenic queens, arising mostly through automixis with central fusion. Sterile castes, male and most (93%) female dispersers are produced sexually. Colony reproduction is usually restricted to a single dispersal of alates with unbiased sex ratio, taking place after 3 years. We conclude that S. minutus benefits from AQS to maximize colony growth rate and alate production within a very short life cycle rather than to extend colony lifespan. This highlights the versatile role of AQS in different cases of its polyphyletic origin.

Chemistry of Social Insects The Institute of Organic Chemistry and Biochemistry Czech Academy of Sciences Flemingovo n 2 166 10 Prague Czech Republic

Chemistry of Social Insects The Institute of Organic Chemistry and Biochemistry Czech Academy of Sciences Flemingovo n 2 166 10 Prague Czech Republic Faculty of Science Charles University Prague Albertov 6 128 43 Prague Czech Republic

Evolutionary Biology and Ecology Université Libre de Bruxelles Av F D Roosevelt 50 1050 Brussels Belgium

IRD Sorbonne Universités UMR 242 Université Pierre et Marie Curie Université Paris Est Créteil Université Paris Diderot CNRS INRA iEES Paris 32 avenue Henri Varagnat 93143 Bondy France LEEC EA4443 Université Paris 13 Sorbonne Paris Cité 99 Avenue J B Clément 93430 Villetaneuse France

Université Paris Est Créteil Université Pierre et Marie Curie CNRS INRA IRD Université Paris Diderot iEES Paris 61 avenue du Général de Gaulle 94010 Créteil France

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