Intraspecific variation in colony founding behavior and social organization in the honey ant Myrmecocystus mendax

Abstract

Persistent cooperation between unrelated reproductives occurs rarely in mature eusocial insect societies, and when present, is frequently geographically constrained. Here we present genetic and behavioral evidence showing that primary polygyny occurs in some, but not all populations of the honey ant Myrmecocystus mendax. Specifically, we found that all mature colonies sampled in a population in the Sierra Ancha Mountains of central Arizona (USA) were polygynous with a relatively high number of queens (average = 6.27), while the majority of mature colonies sampled in the Chiricahua Mountains of southeastern Arizona were monogynous. Field and laboratory observations showed that Chiricahua foundresses are primarily haplometrotic, whereas Sierra Ancha foundresses can be either haplometrotic or facultatively pleometrotic. Nestmate relatedness of mature Sierra Ancha field colonies suggests that the reproductive individuals within these colonies are unrelated, consistent with primary polygyny. In the laboratory, Sierra Ancha foundresses cooperatively established incipient colonies without queen reduction, and colonies with multiple queens produced more minims and workers that may serve the role of repletes (honeypots) than haplometrotic colonies. This was in stark contrast to foundresses from the Chiricahua population, which showed strong aggression when forced to found colonies together in the laboratory. When brood raiding was experimentally induced between laboratory Sierra Ancha colonies, queens from colonies with more workers had a higher survival probability, although in some cases the competing colonies fused and queens from both colonies continued to reproduce. Fusion between incipient ant colonies is a rare phenomenon, but could contribute to the high frequency of polygyny and high queen number in mature colonies in the Sierra Ancha population.

Social insect colonies are more likely to accept unrelated queens when they come with workers

“…The acceptance of alien queens accompanied by workers may be a form of mutualism (West et al, 2021;West et al, 2007), where individuals from both colonies benefit from the association through increased colony size and/or increased genetic diversity. Across social insects larger colonies have better defense abilities against competitors and predators (Eriksson et al, 2019), improved nest thermoregulation (Jones and Oldroyd, 2006;Kadochová and Frouz, 2013;Korb, 2003), higher foraging efficiency (Donaldson-Matasci et al, 2013), and increased division of labor (Ferguson-Gow et al, 2014;Holbrook et al, 2011). Moreover, hosting more genetically diverse individuals within the nest may lead to higher foraging efficiency (Mattila and Seeley, 2007), better colony immunity (Hughes and Boomsma, 2004;Schmid-Hempel and Crozier, 1999;Seeley and Tarpy, 2007), and colony homeostasis (Oldroyd and Fewell, 2007).…”

“…Even though cooperation between alien individuals is widespread across the tree of life (Boucher, 1985;Bronstein, 1994;West et al, 2021), including within eusocial insects (e.g. (Bernasconi and Strassmann, 1999;Eriksson et al, 2019;Field and Leadbeater, 2016;Johnson, 2004;Offenberg et al, 2012;Queller et al, 2000;Trunzer et al, 1998), it is often difficult to disentangle whether eusocial insect colonies host alien queens because they failed to reject them due to constraints in their CHC-based nestmate recognition system (e.g. Reeve, 1989;Suarez et al, 2020;Vásquez and Silverman, 2008; see also Field and Leadbeater, 2016;Suarez et al, 2002), or because the benefits of accepting them outweighted the costs of rejecting them.…”

“…Mutualism also occurs in eusocial insects, like when unrelated young queens associate (usually temporarily) to start a nest (Bernasconi and Strassmann, 1999;Eriksson et al, 2019;Johnson, 2004;Offenberg et al, 2012;Trunzer et al, 1998). Similarly, individuals living in queenright colonies (i.e.…”

“…colonies containing reproductive queens) can benefit from accepting alien queens when doing so increases colony size and/or colony genetic diversity. Larger colonies usually have better nest thermoregulation (Jones and Oldroyd, 2006;Kadochová and Frouz, 2013;Korb, 2003) and foraging efficiency (Donaldson-Matasci et al, 2013), increased division of labor (Ferguson-Gow et al, 2014;Holbrook et al, 2011), and better defense abilities against competitors, predators and brood raiders (Eriksson et al, 2019). And increased genetic diversity can improve colony immunity (Hughes and Boomsma, 2004;Schmid-Hempel and Crozier, 1999;Seeley and Tarpy, 2007), colony homeostasis (Oldroyd and Fewell, 2007) and foraging efficiency (Mattila and Seeley, 2007).…”

Geographic patterns in colonial reproductive strategy inMyrmecina nipponica: Links between biogeography and a key polymorphism in ants

“…Highly social organisms in particular may be well positioned to exploit this advantage because flexibility can be expressed both in the individual and through the extended phenotype of the colony. In social insects for example, intra‐specific polymorphism occurs in social behaviour itself, with various bees and ants exhibiting social/solitary or polygyne/monogyne polymorphisms in different environments (Cronin & Hirata, 2003; Eriksson, Hoelldobler, Taylor, & Gadau, 2019; Field, Paxton, Soro, & Bridge, 2010; Kocher et al., 2014; Purcell, Pellissier, & Chapuisat, 2015). Social insects can also exhibit variability in their reproductive system: the number of reproductive individuals of each sex (notably whether colonies contain one queen [monogyny] or several queens [polygyny], but also the number of times queens mate) has received much attention because it influences colony genetic structure, itself thought to be important for the evolution of sociality (Bourke, 2011; Crozier & Pamilo, 1996; Hamilton, 1964; Hughes, Ratnieks, & Oldroyd, 2008).…”