Intraspecific support for the polygyny-vs.-polyandry hypothesis in the bulldog ant Myrmecia brevinoda

Abstract

The number of queens per colony and the number of matings per queen are the most important determinants of the genetic structure of ant colonies, and understanding their interrelationship is essential to the study of social evolution. The polygyny-vs.-polyandry hypothesis argues that polygyny and polyandry should be negatively associated because both can result in increased intracolonial genetic variability and have costs. However, evidence for this long-debated hypothesis has been lacking at the intraspecific level. Here, we investigated the colony genetic structure in the Australian bulldog ant Myrmecia brevinoda. The numbers of queens per colony varied from 1 to 6. Nestmate queens within polygynous colonies were on average related (r(qq) = 0.171 ± 0.019), but the overall relatedness between queens and their mates was indistinguishable from zero (r(qm) = 0.037 ± 0.030). Queens were inferred to mate with 1-10 males. A lack of genetic isolation by distance among nests indicated the prevalence of independent colony foundation. In accordance with the polygyny-vs.-polyandry hypothesis, the number of queens per colony was significantly negatively associated with the estimated number of matings (Spearman rank correlation R = -0.490, P = 0.028). This study thus provides the rare intraspecific evidence for the polygyny-vs.-polyandry hypothesis. We suggest that the high costs of multiple matings and the strong effect of multiple mating on intracolonial genetic diversity may be essential to the negative association between polygyny and polyandry and that any attempt to empirically test this hypothesis should place emphasis upon these two key underlying aspects.

Reproductive conflicts in polyandrous and polygynous ant Formica sanguinea

“…2007; Schlüns et al. 2009), our present results are similar to those reported by Qian et al. (2011) and show that the level of polyandry in F. sanguinea is significantly higher under monogyny than polygyny.…”

“…That relationship supports the hypothesis that the increased genotypic diversity within colonies caused by either polyandry or polygyny is beneficial, but that these are alternative breeding strategies because polyandry may also be costly to the queens. To what extent the negative correlation of polyandry and polygyny applies to colonies within a population must depend on the patterns of and costs associated with queen mating, dispersal and colony founding (Qian et al. 2011).…”

Colony life history and lifetime reproductive success of red harvester ant colonies

“…Sundstr€ om 1993; Chapuisat & Keller 1999;Bargum, Helantera & Sundstrom 2007), and queen number (e.g. Ross et al 1997;Chapuisat, Bocherens & Rosset 2004;Qian et al 2011).…”

Colony genetic structure in the Australian jumper ant Myrmecia pilosula

“…This hypothesis has been largely controversial because it has rarely gained any empirical support at the intraspecific level (Bekkevold et al, 1999;Chapuisat, 1998;Hammond et al, 2001;Kellner et al, 2007;Pedersen and Boomsma, 1999a;Trontti et al, 2005); these findings are consistent with this study of M. pilosula. However, we did find such a significantly negative association in our recent investigation into the colony genetic structure of the congeneric bulldog ant M. brevinoda (Qian et al, 2011b). By reviewing all available empirical tests of this hypothesis, we proposed that the high mating costs and the strong effect of multiple matings on intracolonial genetic diversity may be essential to such a negative association at the intraspecific level.…”

“…It is the first time that the rare cooccurrence of polygyny and high polyandry has been found in the M. pilosula species group. The overall level of polyandry is lower than that in the congeneric giant bulldog ant M. brevinoda (Qian et al, 2011b), comparable to that in the congeneric brown bulldog ant M. pyriformis (Sanetra, 2011), but higher than that in the monogynous consubfamilial dinosaur ant Nothomyrmecia macrops (Sanetra and Crozier, 2001). In ants, there are two main strategies of colony foundation, i.e., independent colony foundation (ICF) by solitary queens and dependent colony foundation (DCF) when the queen starts a colony with the help of workers from her natal colony (reviewed by Fernández-Escudero et al, 2001;Johnson, 2010;Peeters and Molet, 2009).…”