Multiple paternity or multiple queens: two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera

Abstract

Understanding the evolution of multiple mating by females (polyandry) is an important question in behavioural ecology. Most leading explanations for polyandry by social insect queens are based upon a postulated fitness benefit from increased intracolonial genetic diversity, which also arises when colonies are headed by multiple queens (polygyny). An indirect test of the genetic diversity hypotheses is therefore provided by the relationship between polyandry and polygyny across species, which should be negative if the genetic diversity hypotheses are correct. Here, we conduct a powerful comparative investigation of the relationship between polyandry and polygyny for 241 species of eusocial Hymenoptera (ants, bees and wasps). We find a clear and significant negative relationship between polyandry and polygyny after controlling for phylogeny. These results strongly suggest that fitness benefits resulting from increased intracolonial genetic diversity have played an important role in the evolution of polyandry, and possibly polygyny, in social insects.

Beyond promiscuity: mate-choice commitments in social breeding

“…Thus, ants, eusocial bees and eusocial wasps tend to have either 100 per cent single mating, or some mixture of colonies headed by a monandrous or mildly polyandrous queen, or 100 per cent (usually high) polyandry of queens [16,85,87] (figure 2). There is now reasonable consensus about the evolution of obligate multiple mating having been driven by benefits related to enhanced genetic diversity among workers (proposed by [89,90] and reviewed by [85,87,[91][92][93]), but what has driven the convergent evolution of facultative multiple mating has remained enigmatic. It is tempting to speculate that this mating system evolved to allow females to correct suboptimal first inseminations, but considerable research effort will be required to unravel the interaction between sperm transfer, mating plug efficiency and female sperm storage responses, which seems a tall order as almost no eusocial species with facultative multiple mating are known to mate under laboratory conditions.…”

Polygyny in the nest-site limited acacia-ant Crematogaster mimosae

“…Simultaneous polygyny and polyandry have been shown in some ant species (Pamilo, 1993;Pedersen and Boomsma, 1999b;Kellner et al, 2007;Trontti et al, 2007), but Keller and Reeve (1994) suggested that this condition is rare because potential benefits of genetic variability could be fully achieved by either polyandry or polygyny. Although Schmid-Hempel and Crozier (1999) showed that ants of this type are not unusual, Hughes et al (2008) and Kronauer and Boomsma (2007) found strong negative relationships between polygyny and mating frequency in ants. Based on direct observation of colony formation, Stanton et al (2002) suggested that C. mimosae colonies begin with a single queen, and hence queens may mate multiply to ensure within-colony genetic diversity in the initial stages of colony development.…”

“…The presence of multiple reproductive queens often decreases the relatedness of colony members and may reduce the inclusive fitness returns for non-reproductive individuals by encouraging their cooperation with less related nestmates (Hamilton, 1964;Nonacs, 1988;Ross, 1988;Keller, 1995). Factors that have been shown to promote polygyny despite these costs include intraspecific brood raiding during colony founding (Rissing and Pollock, 1987;Herbers, 1993;Sommer and Hölldobler, 1995;Bernasconi and Strassmann, 1999), nestsite limitation due to habitat saturation (Herbers, 1986;Seppä et al, 1995;Puntilla, 1996;Pedersen and Boomsma, 1999a;Feldhaar et al, 2005), frequent habitat disturbance (Hölldobler and Wilson, 1977), low queen lifespan compared to colony survivorship (Nonacs, 1988), and the advantages of increased genetic diversity within colonies Boomsma, 2004, 2006;Wiernasz et al, 2004Wiernasz et al, , 2008Hughes et al, 2008), although this can also be accomplished through multiple matings. Primary polygyny, the founding of colonies by multiple, usually unrelated queens, can increase initial worker production, potentially strengthening colony defenses soon after colony founding (Rissing and Pollock, 1987;Sommer and Hölldobler, 1995;Bernasconi and Strassmann, 1999).…”

The effects of genotype, caste, and age on foraging performance in leaf-cutting ants

“…Suggested benefits that may explain polyandry include direct benefits, such as sperm provision, nuptial gifts, and paternal care, and indirect genetic benefits, such as trading up, the dilution of genetic incompatibility, and increased offspring genetic diversity (Arnqvist and Nilsson 2000; Jennions and Petrie 2000;Simmons 2005). In contrast to most other animals, monandry (females inseminated by only a single male) is the most common and ancestral state in social insects, with females (queens) in only a third of species exhibiting some level of polyandry (Hughes et al 2008a(Hughes et al , 2008b. However, some of these are notable for having evolved exceptionally high or apparently obligate levels of polyandry.…”