RESEARCH ARTICLE Distribution and origin of intraspecific social variation in the California harvester ant Pogonomyrmex californicus R. Overson 1 • J. Fewell 2 • J. Gadau 2 Received: 18 August 2015 / Revised: 7 July 2016 / Accepted: 12 July 2016 / Published online: 25 July 2016 Ó International Union for the Study of Social Insects (IUSSI) 2016 Abstract The California seed harvester ant Pogonomyrmex californicus exhibits striking differences in queen behavior and colony organization throughout its range. Most popu- lations show the likely ancestral condition of single-queen colonies (monogyny). However, in one known population, cooperation between queens during colony founding (pleometrosis) occurs, and is suspected to persist to the mature colony stage (primary polygyny). To better under- stand this variation in social phenotype, we estimate relatedness among co-foundresses, measure the frequency of polygyny in adult colonies across three focal populations, and assess population genetic structure between popula- tions. We additionally measure queen mating frequency (polyandry) across focal populations. With few possible exceptions, queens within pleometrotic associations are unrelated. We demonstrate a correlation between pleomet- rosis in incipient colonies and polygyny in adult colonies at the population level. Nuclear microsatellites and mtDNA barcoding indicate significant structure between focal pop- ulations. Queens from all three focal populations engage in relatively high levels of polyandry. These findings, when examined with previous data demonstrating that pleomet- rosis leads to polygynous colonies in the laboratory, strongly suggest that the same occurs in nature. However, the possibility of additional queen adoption in adult colonies (secondary polygyny) is not excluded. Thus, polygynous P. californicus colonies potentially represent long-term asso- ciations of unrelated family groups, containing multiple unrelated queens and their mixed-paternity offspring. Due to its pronounced variation in social behavior, P. califor- nicus provides a unique opportunity to examine the evolutionary history and genetic underpinnings of cooper- ation among non-relatives, a strategy of intense interest in behavioral ecology. Keywords Pogonomyrmex Á Primary polygyny Á Pleometrosis Á Cooperation Á Population genetics Á Biogeography Introduction Much research has been carried out to understand the dynamics of cooperation between relatives described by kin selection, a primary driver of cooperative sociality (Hamilton 1964; West-Eberhard 1975; Creel and Rabenold 1994; Bourke and Franks 1995; Queller and Strassmann 1998; Bernasconi and Strassmann 1999; Alonso and Schuck-Paim 2002; Clutton-Brock 2002; Baglione et al. 2003; Griffin and West 2003). The advent of molecular tools, however, has led to the discovery of long-overlooked interactions of cooperating non-relatives (Dugatkin and Mesterton-Gibbons 1996; Balshine-Earn et al. 1998; Quel- ler et al. 2000; Aviles 2002; Clutton-Brock 2002; Dugatkin 2002; Toquenaga 2005; Clutton-Brock 2009; Bshary 2010; Cheney et al. 2010). Efforts are underway, among consid- erable debate, to establish an integrative understanding of Electronic supplementary material The online version of this article (doi:10.1007/s00040-016-0497-8) contains supplementary material, which is available to authorized users. & R. Overson rickoverson@gmail.com 1 Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, IL 60022, USA 2 School of Life Sciences and Center for Social Dynamics and Complexity, Arizona State University, Tempe, AZ 85287-4501, USA Insect. Soc. (2016) 63:531–541 DOI 10.1007/s00040-016-0497-8 Insectes Sociaux 123