The foundress’s dilemma: group selection for cooperation among queens of the harvester ant, Pogonomyrmex californicus

Abstract

The evolution of cooperation is a fundamental problem in biology, especially for non-relatives, where indirect fitness benefits cannot counter within-group inequalities. Multilevel selection models show how cooperation can evolve if it generates a group-level advantage, even when cooperators are disadvantaged within their group. This allows the possibility of group selection, but few examples have been described in nature. Here we show that group selection can explain the evolution of cooperative nest founding in the harvester ant Pogonomyrmex californicus. Through most of this species’ range, colonies are founded by single queens, but in some populations nests are instead founded by cooperative groups of unrelated queens. In mixed groups of cooperative and single-founding queens, we found that aggressive individuals had a survival advantage within their nest, but foundress groups with such non-cooperators died out more often than those with only cooperative members. An agent-based model shows that the between-group advantage of the cooperative phenotype drives it to fixation, despite its within-group disadvantage, but only when population density is high enough to make between-group competition intense. Field data show higher nest density in a population where cooperative founding is common, consistent with greater density driving the evolution of cooperative foundation through group selection.

Towards a mechanistic foundation of evolutionary theory

“…as colonies of insects. In particular, group selection may be an important driver for the evolution of eusociality (Nowak et al, 2010;Shaffer et al, 2016;Wilson and Wilson, 2008). Group level birth and death events, and hence group selection, may also be very important for the evolution of multicellularity from aggregations of singlecelled organisms (Hammerschmidt et al, 2014;Ratcliff et al, 2012).…”

Collective aggressiveness limits colony persistence in high‐ but not low‐elevation sites at Amazonian social spiders

“…Social organisms provide an interesting case study for evolutionary ecologists, because trait differences occur at both the individual‐level and between groups, in terms of their collective traits (Bengston & Jandt, ; Jandt et al., ; Wray & Seeley, ). Like individual traits, a growing body of evidence conveys that group traits are often associated with group success (Gordon, ; Shaffer et al., ; Wray, Mattila, & Seeley, ), and that these links can vary between environments (Pruitt & Goodnight, ; Pruitt et al., ). Site‐specific selection may therefore contribute to biodiversity by promoting intraspecific variation and local adaptation in group‐level traits.…”

Foundress Number, But Not Queen Size or Boldness, Predicts Colony Life-History in Wild Paper Wasps

“…This is because the initial work and investment of a singleton foundress (e.g., colony establishment, brood care, defence) can strongly influence in a colony’s development, behavior, and functioning (e.g., Wright et al 2017). This is true of highly eusocial species as well (Fewell & Page, 1999; Shaffer, Sasaki, Haney, Janssen, Pratt & Fewell, 2016), but we predict such effects will diminish as colonies grow and develop in highly eusocial species. Second, in multi-queen founding species, the number of foundresses is likely to influence colony life-history trajectories (Field, Solis, Queller & Strassmann, 1998; Tibbetts & Reeve, 2000).…”