Received: 12 January 2018 | Revised: 10 May 2019 | Accepted: 17 May 2019 DOI: 10.1111/mec.15137 ORIGINAL ARTICLE High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp Polistes canadensis Robin J. Southon1 | Emily F. Bell1 | Peter Graystock1,2 | Christopher D. R. Wyatt1,3,4 | Andrew N. Radford1 | Seirian Sumner1,5 1School of Biological Sciences, University of Bristol, Bristol, UK Abstract 2Department of Life Sciences, Imperial Explaining the evolution of helping behaviour in the eusocial insects where nonrepro‐ College London, London, UK ductive (“worker”) individuals help raise the offspring of other individuals (“queens”) 3EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation remains one of the most perplexing phenomena in the natural world. Polistes paper (CRG), The Barcelona Institute of Science wasps are popular study models, as workers retain the ability to reproduce: such and Technology, Barcelona, Spain totipotency is likely representative of the early stages of social evolution. Polistes is 4Universitat Pompeu Fabra (UPF), Barcelona, Spain thought to have originated in the tropics, where seasonal constraints on reproduc‐ 5Centre for Biodiversity and Environmental tive options are weak and social groups are effectively perennial. Yet, most Polistes Research, Department of Genetics, research has focused on nontropical species, where seasonality causes family groups Evolution and Environment, University College London, London, UK to disperse; cofoundresses forming new nests the following spring are often unre‐ lated, leading to the suggestion that direct fitness through nest inheritance is key in Correspondence Seirian Sumner, School of Biological the evolution of helping behaviour. Here, we present the first comprehensive genetic Sciences, University of Bristol, Bristol BS8 study of social structure across the perennial nesting cycle of a tropical Polistes— 1TQ, UK. Email: [email protected] Polistes canadensis. Using both microsatellites and newly developed single nucleo‐ tide polymorphism markers, we show that adult cofoundresses are highly related and Funding information Natural Environment Research Council, that brood production is monopolized by a single female across the nesting cycle. Grant/Award Number: NE/K011316/1 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. KEYWORDS inclusive fitness, Polistes, relatedness, reproductive skew, single nucleotide polymorphisms 1 | INTRODUCTION individuals produce young (West, Pen, & Griffin, 2002). In extreme cases, only one or a few group members reproduce whilst other Societal living entails both benefits and costs for individuals (Krause (nonreproducing) individuals assist in rearing the young. Such repro‐ & Ruxton, 2002). Unless clonal, one such cost is the conflict over ductive division of labour, with high reproductive skew, is found in reproduction that exists between group members when only some a range of social taxa (Cant & Johnstone, 2008; Kokko & Johnstone, 1999; Wilson, 1971). Determining how reproduction is divided Robin J. Southon and Emily F. Bell equally contributed to this work. among conspecific group members, and why individuals forgo inde‐ pendent breeding to be a helper, is fundamental for understanding Molecular Ecology. 2019;28:3271–3284. wileyonlinelibrary.com/journal/mec © 2019 John Wiley & Sons Ltd | 3271 3272 | SOUTHON ET AL. the evolution of sociality (Keller & Reeve, 1999; West, Griffin, & are asynchronous, and reproductively potent individuals can initi‐ Gardner, 2007). ate new nests and mate at any time of the year (O'Donnell & Joyce, Nonreproductive group members may help because of future 2001; Pickering, 1980; West‐Eberhard, 1969). Therefore, females in direct and/or current indirect fitness benefits. Where group relat‐ tropical species potentially have access to better information (and edness is low, or less than the population average, helping can be different mechanisms) for selecting relatives to nest with than do explained by immediate or delayed direct fitness benefits. These temperate species (Dani et al., 2004; Dapporto et al., 2004; Sumana include the advantages accrued from group augmentation and the et al., 2005; Tibbetts & Injaian, 2013). Polistes is thought to have potential to inherit the breeding position or territory (Clutton‐Brock, originated in the tropics (Carpenter, 1996; Santos, Payne, Pickett, & 2009). When group members are closely related, the costs of helping Carpenter, 2015), and two‐thirds of species in this genus are tropi‐ can be balanced by indirect (kin‐selected) fitness benefits (Queller cal (West‐Eberhard, 1969). The impact of climate and environmental & Strassmann, 1998), as proposed by Hamilton (1964). Changes in variation on sociality has recently been noted in cooperatively breed‐ group composition that alter average group relatedness have po‐ ing birds, bees and wasps (Cockburn & Russell, 2011; Cronin, Bridge, tential implications for the relative payoffs of helping versus repro‐ & Field, 2011; Field, Paxton, Soro, & Bridge, 2010; Fucini, Bona, ducing. Such changes can arise due to both intrinsic (e.g., intragroup Mola, Piccaluga, & Lorenzi, 2009; Jetz & Rubenstein, 2011; Richards, competition and turnover of breeders) and extrinsic (e.g., seasonal 2000; Sheehan et al., 2015). However, we lack detailed analyses of constraints and fluctuating resource availability) factors (Armitage, the genetic structure and fitness strategies employed in Polistes spe‐ 2007; Koštál, 2006; McCracken & Wilkinson, 2000; Wittemyer, cies across latitudinal gradients, especially for the foundress period Getz, Vollrath, & Douglas‐Hamilton, 2007). Tests of how environ‐ and for tropical species (see summary in Appendix S1). Specifically, mental conditions influence reproductive options, and the resulting genetic data on foundress nests are limited to seven species (four fitness payoffs, are needed for a full understanding of the relative species in temperate regions, three in subtropical) and entirely miss importance of direct and indirect fitness for helpers (Bourke, 2014). tropical species. This is a critical gap in our understanding of social The simple societies of Polistes paper wasps, where there is a evolution as it is the tropical—as opposed to the temperate—species division of labour in behavioural roles but all individuals (to a degree) of Polistes that are likely to experience ecological conditions similar retain the potential to reproduce, likely exhibit similar traits to those to those under which sociality first evolved in this genus. found in the early stages of eusocial evolution (Danforth & Eickwort, Here, we examine genetic structure and reproductive partitioning 1997; Jeanne, 1980; Keller, 2003; Reeve, 1991; West‐Eberhard, in societies of the tropical paper wasp Polistes canadensis, an emerging 1969). Studies to date have indicated the importance of both direct model species for Polistes research (Ferreira et al., 2013; Jeanne, 1979; and indirect fitness benefits for Polistes sociality (Boomsma, 2007; Patalano et al., 2015; Pickering, 1980; Sumner, Kelstrup, & Fanelli, Field & Leadbeater, 2016; Leadbeater, Carruthers, Green, Rooser, & 2010; Sumner, Lucas, Barker, & Isaac, 2007; Sumner, Pereboom, & Field, 2011; Queller et al., 2000). For example, in the best‐studied Jordan, 2006; West‐Eberhard, 1986). New nests are cofounded by species of the genus, Polistes dominula, direct fitness via nest in‐ several females (Miller et al., 2018; Pickering, 1980), yet it is unknown heritance has been shown to explain helping behaviour during the whether these females are often of low relatedness or unrelated, as group‐founding (foundress) stage, when group members are often in temperate species (Appendix S1). The República de Panamá, in unrelated (Field & Leadbeater, 2016; Kokko & Johnstone, 1999; the central range for P. canadensis, experiences seasonal variation in Leadbeater et al., 2011; Queller et al., 2000; Strassmann et al., 1989; the form of wet and dry periods, but there is no enforced overwin‐ Zanette & Field, 2008). By contrast, indirect fitness from raising sib‐ tering diapause period. All stages of the nesting cycle can be found lings explains helping behaviour in later stages of the nesting cycle together throughout the year (including the dry season) (Pickering, of P. dominula, where the mothers of the helpers monopolize repro‐ 1980), permitting their simultaneous study under the same environ‐ duction (Field, Solís, Queller, & Strassmann, 1998; Peters, Queller, mental conditions. These life history and environmental traits allow us Strassmann, & Solís, 1995; Queller, Peters, Solís, & Strassmann, to investigate whether species that have weak/no seasonally induced 1997; Queller & Strassmann, 1998; Reeve & Keller, 2001; Seppä, changes in group membership consist of highly related cofoundresses. Queller, & Strassmann, 2002). However, P. dominula is a temperate Closely related cofoundresses are predicted to exhibit little conflict species where newly mated young queens undergo an obligatory over reproduction as the