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.

Highlights

  • Queen number is a key aspect of social organization in ant colonies and shows both inter- and intraspecific variation in natural populations (Rissing and Pollock 1988; Hölldobler and Wilson 1990; Bernasconi and Strassmann 1999; Overson et al 2011; Helms and Cahan 2012)

  • We show that queens from the Sierra Ancha Mountains of central Arizona exhibit mutual tolerance, and that primary polygyny and colony fusion are present at this site

  • The sociogenetic analyses and laboratory experiments described here demonstrate that M. mendax populations in the Chiricahua (CHI) and Sierra Ancha Mountains (SIE) differ greatly in their social organization as mature colonies, in their colony founding strategy, and in the behaviors exhibited during interactions between queens and between colonies

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Summary

Introduction

Queen number is a key aspect of social organization in ant colonies and shows both inter- and intraspecific variation in natural populations (Rissing and Pollock 1988; Hölldobler and Wilson 1990; Bernasconi and Strassmann 1999; Overson et al 2011; Helms and Cahan 2012). The simplest social organization of an ant colony consists of one foundress starting a new colony alone (haplometrosis) and monopolizing reproduction thereafter (monogyny). In a number of taxa, monogynous colonies can later adopt additional queens, thereby becoming secondarily polygynous. Colonies are cooperatively established by multiple, usually unrelated foundresses (pleometrosis). Polygyny that arises from these associations is often short-lived (Tschinkel 1992; Bernasconi and Strassmann 1999). All but one queen are subsequently culled following the emergence of the first workers, resulting in secondary monogyny

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