The potential for worker reproduction in the ant Aphaenogaster cockerelli and its absence in the field

Abstract

A reproductive division of labor between subordinates and established reproductives is a hallmark of eusociality. In most groups, however, workers retain some reproductive capabilities. Across insect societies, measures of successful worker reproduction in the presence of a queen, with few exceptions, indicate that worker reproduction is kept at very low levels. There are, however, certain colony-level characteristics that may influence the degree to which worker reproduction is promoted, such as queen number, queen mating frequency, and physical presence of a queen in species with multiple nesting sites (polydomy). In this study, the level of worker reproduction in field colonies of the ant species Aphaenogaster cockerelli was measured. A. cockerelli is a monogynous and polydomous species, so worker reproduction across nesting sites was investigated. None of the 297 males sampled provided any evidence of worker reproduction. Worker reproduction would have been detectable if it was present at or above a level of 1.5 % of the total males per colony. An effective mating frequency for queens of this species was found to be 1.03. Although A. cockerelli colonies have many colonylevel factors potentially promoting worker reproduction (workers with active, trophic egg-producing ovaries, a single singly-mated queen, workers who are physically separated from the queen), it is evident that worker reproduction is highly regulated. Synthesizing the extensive amount of policing and fertility signaling data previously reported on this species, A. cockerelli is presented as case study for how worker reproduction is repressed and cooperation is maintained in insect societies.

Substantial direct fitness gains of workers in a highly eusocial ant

“…The genotypes of queens and workers from queenright field colonies suggest a rather instable structure of the studied T. crassispinus population, with frequent queen turnovers, colony usurpations, and fusions, similar to what has been observed in its sibling species T. nylanderi (Foitzik & Heinze, 1998Foitzik, Sturm, Pusch, d'Ettorre, & Heinze, 2007;Strätz & Heinze, 2004). Furthermore, queenless field colonies might have lost their queen or be fragments of queenright colonies (Cao, 2013;Debout et al, 2007;Smith et al, 2012;Strätz & Heinze, 2004). This population fluidity appears to result from high queen mortality (J.…”

“…This reveals a high realized reproductive potential of T . crassispinus workers compared to other social insect species (ants: Helanterä & Sundström, 2007b; Smith et al., 2012; Walin et al., 1998; honey bees and wasps: Foster, Ratnieks, Gyllenstrand, & Thorén, 2001; Ratnieks, 1993) including many congeneric species, in which the development of worker‐produced eggs is prevented by worker policing or queen pheromones (Helanterä & Sundström, 2007a; Stroeymeyt et al., 2007; Walin et al., 1998; Walter et al., 2011). Previous observations had shown that workers interact aggressively by antennal boxing and biting in both queenless and queenright colonies (El‐Shehaby et al., 2012).…”

“…nylanderi (Foitzik & Heinze, 1998, 2000; Foitzik, Sturm, Pusch, d’Ettorre, & Heinze, 2007; Strätz & Heinze, 2004). Furthermore, queenless field colonies might have lost their queen or be fragments of queenright colonies (Cao, 2013; Debout et al., 2007; Smith et al, 2012; Strätz & Heinze, 2004). This population fluidity appears to result from high queen mortality (J. Giehr, unpublished), very high nest densities, the fragility of nest sites, and presumably also a nestmate recognition system strongly based on environmental cues (Foitzik et al., 2007; Heinze, Foitzik, Hippert, & Hölldobler, 1996).…”

“…This all suggests that workers of many advanced eusocial Hymenoptera are also under selection to maximize their direct fitness. Nevertheless, most genetic data document only a small contribution of workers to the male offspring of the colony (e.g., Smith, Overson, Hölldobler, & Gadau, 2012; Visscher, 1989; Walin, Sundström, Seppä, & Rosengren, 1998; Wenseleers et al., 2004; Wenseleers & Ratnieks, 2006). For example, in a meta‐analysis, Hammond and Keller (2004) reported that in more than 2/3 of all studied species, less than 10% of the males were worker offspring.…”