Behavioral Ecology The ofcial journal of the ISBE International Society for Behavioral Ecology Original Article Horizontal partner exchange does not preclude stable mutualism in fungus-growing ants Jack Howe , Morten Schiøtt and Jacobus J. Boomsma Centre for Social Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark Received 14 June 2018; revised 19 October 2018; editorial decision 13 November 2018; accepted 27 November 2018; Advance Access publication 26 December 2018. Vertical symbiont transmission tends to stabilize mutualisms by aligning the reproductive interests of cooperating species. The attine ants conform well to this principle because all species are nutritionally dependent on vertically transmitted and clonally propagated fungal cultivars. Multiple mechanisms expressed by both partners constrain cultivar transmission between established colonies, but these appear not to preclude horizontal transfer during colony founding, consistent with multiple phylogenetic analyses indicating at least occasional horizontal transfer. The ecological and evolutionary impact of transfers is unknown because, although they can be induced in laboratory experiments, they remain undocumented in natural colonies. In a large-scale field study, we manipulated clusters of newly founded nests and their still portable gardens in two sympatric species of Acromyrmex leaf-cutting ants. This cre- ated mosaics of intact nests, queens without a cultivar, and cultivars without a tending queen. We tracked the movements of queens and cultivars through direct observation and microsatellite analysis, respectively. This showed that horizontal acquisition of incipient gardens is surprisingly common because queens actively searched for replacement cultivars and often adopted orphaned gardens. However, these horizontal cultivar exchanges are unlikely to destabilize obligate farming mutualisms when they are restricted to the founding stage, as colonies eventually commit to a single cultivar clone, irreversibly aligning the partners’ fitness interests before colonies reproduce. Key words: attine ants, mutualism, symbiont transmission, symbiosis. INTRODUCTION That cooperation across species boundaries is prevalent and rarely succumbs to corruption or other forms of cheating requires an explanation (Herre et al. 1999; Sachs et al. 2004; Foster and Wenseleers 2006). There is considerable consensus highlighting the transmission mode of potential cooperators as being particularly important in determining the evolutionary stability of symbio- ses and in limiting the potential benefts to be gained by exploit- ative cells or individuals (Frank 1994; Sachs et al. 2004; Foster and Wenseleers 2006; Douglas 2008). Vertical transmission tends to align the reproductive interests of host and symbiont and to create high relatedness within symbiont populations associated with single hosts (Frank 1997), which likely explains why ancient, highly coop- erative, and coevolved symbionts such as eukaryotic mitochondria and chloroplasts show strict vertical transmission of single clones (Birky 1995). Comparative data across extant symbioses further indicate that vertically inherited symbionts generally contribute more to host ftness (Fisher et al. 2017), and that regimes of verti- cal inheritance select for reduced virulence and increased coopera- tion in both mutualists and pathogens (Bull et al. 1991; Frank 1996; Stewart et al. 2005; Sachs and Wilcox 2006). By contrast, even low levels of horizontal transmission could lead to divergent host and symbiont interests and select for symbiont traits that actively pur- sue enhanced rates of horizontal transmission at the expense of the host (Anderson and May 1982; Ewald 1987; Frank 1996). Any mutualism, therefore, is best understood as the mutual exploitation of partners, with horizontal transmission facilitating higher degrees of exploitation compared to vertically inherited symbionts (Herre et al. 1999). In light of horizontal transmission selecting for the expression of virulence, that is, increased exploitation (Frank 1996), it seems paradoxical that several evolutionarily old and stable mutualisms rely exclusively on horizontal symbiont acquisition. In the fungus- growing termites, for example, newly founded colonies typically acquire their obligate cultivar by collecting a diversity of hap- lospores produced by sexual reproduction via mushrooms of the Address correspondence to J. Howe. E-mail: jack.howe@bio.ku.dk; J.J. Boomsma. E-mail: JJBoomsma@bio.ku.dk © The Author(s) 2018. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com Behavioral Ecology (2019), 30(2), 372–382. doi:10.1093/beheco/ary176 Downloaded from https://academic.oup.com/beheco/article/30/2/372/5261069 by guest on 17 June 2022