Identifying the transition between single and multiple mating of queens in fungus-growing ants

Abstract

Obligate mating of females (queens) with multiple males has evolved only rarely in social Hymenoptera (ants, social bees, social wasps) and for reasons that are fundamentally different from those underlying multiple mating in other animals. The monophyletic tribe of ('attine') fungus-growing ants is known to include evolutionarily derived genera with obligate multiple mating (the Acromyrmex and Atta leafcutter ants) as well as phylogenetically basal genera with exclusively single mating (e.g. Apterostigma, Cyphomyrmex, Myrmicocrypta). All attine genera share the unique characteristic of obligate dependence on symbiotic fungus gardens for food, but the sophistication of this symbiosis differs considerably across genera. The lower attine genera generally have small, short-lived colonies and relatively non-specialized fungal symbionts (capable of living independently of their ant hosts), whereas the four evolutionarily derived higher attine genera have highly specialized, long-term clonal symbionts. In this paper, we investigate whether the transition from single to multiple mating occurred relatively recently in the evolution of the attine ants, in conjunction with the novel herbivorous 'leafcutter' niche acquired by the common ancestor of Acromyrmex and Atta, or earlier, at the transition to rearing specialized long-term clonal fungi in the common ancestor of the larger group of higher attines that also includes the genera Trachymyrmex and Sericomyrmex. We use DNA microsatellite analysis to provide unambiguous evidence for a single, late and abrupt evolutionary transition from exclusively single to obligatory multiple mating. This transition is historically correlated with other evolutionary innovations, including the extensive use of fresh vegetation as substrate for the fungus garden, a massive increase in mature colony size and morphological differentiation of the worker caste.

Patterns of male parentage in the fungus-growing ants

“…One such comparative analysis was recently completed for the vespine wasps (Foster et al 1999. Here we present a similar analysis for the attine fungus-growing ants, another tribe of social insects for which the phylogeny is known (Schultz and Meier 1995;Wetterer et al 1998) and where multiple queen-mating is restricted to the most derived terminal genera, the Acromyrmex and Atta leafcutter ants (Villesen et al 1999(Villesen et al , 2002b. All species of leafcutter ants so far investigated have effective queenmating frequencies of two or above (Fjerdingstad et al 1998;Bekkevold et al 1999;Boomsma et al 1999;Fjerdingstad and Boomsma 2000), so that worker reproduction is not expected to occur in queenright colonies (Ratnieks 1988).…”

“…All species of leafcutter ants so far investigated have effective queenmating frequencies of two or above (Fjerdingstad et al 1998;Bekkevold et al 1999;Boomsma et al 1999;Fjerdingstad and Boomsma 2000), so that worker reproduction is not expected to occur in queenright colonies (Ratnieks 1988). However, representatives of the lower attines (Villesen et al 1999;Murakami et al 2000) and the basal genera of the higher attines, Trachymyrmex and Sericomyrmex (Villesen et al 2002b), are exclusively or predominantly singly mated, so that the conflict over male production may be expressed and may at least be partly won by the workers. To test this hypothesis, we have determined the maternity of males in a sample of colonies from eight different species of non-leafcutting fungusgrowing ants.…”

Comparative Analysis of Worker Reproduction and Policing in Eusocial Hymenoptera Supports Relatedness Theory

“…Sweat bees were added as basal to the long-tongued bees (Alexander and Michener 1995). For honeybees, leafcutter ants, and bumblebees, the molecular phylogenies of Arias and Sheppard (2005), Villesen et al (2002), and Kawakita et al (2004) were used. Relationships among the Polistinae wasps followed the combined morphological and molecular phylogeny of Arévalo et al (2004).…”

The ejaculatory biology of leafcutter ants

“…However, mating plugs are unlikely to have a similar function in A. colombica. The AGs in this species are relatively small compared to the AGs in phylogenetically more basal attine ants that always have single paternity among offspring (Baer and Boomsma, 2004;Villesen et al, 2002). If mating plug size is linearly related to AG size, then the monandrous attine ants are expected to produce relatively large plugs that are successful in preventing re-mating, whereas A. colombica males produce relatively small plugs that fail to prevent access of ejaculates of additional males to the queen's reproductive tract.…”