Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants

Abstract

Division of labor is fundamental to the success of all societies. The most striking examples are the physically polymorphic worker castes in social insects with clear morphological adaptations to different roles. These polymorphic worker castes have previously been thought to be a classic example of nongentically controlled polymorphism, being mediated entirely by environmental cues. Here we show that worker caste development in the leaf-cutting ant Acromyrmex echinatior has a significant genetic component. Individuals of different patrilines within the same colony differ in their propensities to develop into minor or major workers. The mechanism appears to be plastic, with caste destiny resulting from interplay between nurture and nature. Unlike the few other recently discovered examples of a genetic influence on caste determination, the present result does not relate to any rare or exceptional circumstances, such as interspecific hybridization. The results suggest that a significant role of genetics may have been overlooked in our understanding of other complex polymorphisms of social insects.

The ejaculatory biology of leafcutter ants

“…Polyandry increases genetic variation among the worker offspring, which in turn enhances a colony's collective performance in division of labor or disease resistance Cole and Wiernasz, 1999;Hughes et al, 2003;Jaffé et al, 2007;Jones et al, 2004;Mattila and Seeley, 2007;Oldroyd and Fewell, 2007;Smith et al, 2008). Such genetic diversity benefits are maximized by sperm mixing in the queen spermatheca and random sperm use, consistent with empirical data (Brodschneider et al, 2012;Franck et al, 1999;Holman et al, 2011;Stürup et al, 2014).…”

Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor

“…Recently, however, a genetic basis of worker polymorphism within colonies has been documented in some species with distinct morphological castes. Workers of different patrilines differ significantly in their propensities to develop into a certain worker caste in Acromyrmex echinatior (Hughes et al 2003) and Pogonomyrmex badius (Rheindt et al 2005), whereas matrilines influence worker caste determination in Camponotus consobrinus (Fraser et al 2000). This lends support to the hypothesis that increased genetic diversity within colonies results in more polymorphic workers, which in turn could facilitate genetic polyethism by increasing phenotypic plasticity at the colony level (Crozier & Page 1985).…”

“…Workers from different patrilines reportedly differ in size in F. selysi, with a heritability estimate of 0.26 (Schwander et al 2005). In P. badius (Rheindt et al 2005) and A. echinatior (Hughes et al 2003), two species with distinct worker castes, larvae of different patrilines within the same colony differ in their propensities to develop into minor or major workers. A genetic influence on worker size was also reported in polygynous colonies, with workers from different matrilines differing in size in F. selysi (Schwander et al 2005) and C. consobrinus (Fraser et al 2000).…”

“…To our knowledge, two such studies were performed in ants. In the leaf-cutting ant, A. echinatior, the genetic component to worker caste polymorphism described above is associated with a division of labour, with small workers specializing in intranidal tasks and large workers in foraging (Hughes et al 2003). A significant genetic component to worker size was also reported in the wood ant, Formica selysi, a species with no distinct morphological castes (Schwander et al 2005).…”

“…While the effect of genetic diversity on worker task efficiency and colony productivity in social insects still remains debated (see Rosset et al 2005 and references therein), several empirical tests of the hypothesis have shown that genetic variability increases polyethism. For instance, workers belonging to certain patrilines show a higher tendency to perform certain tasks such as foraging, recruiting, guarding, stinging, or nest-cleaning in the honeybee (Frumhoff & Baker 1988;Robinson & Page 1988, 1989Page et al 1989Page et al , 1995Oldroyd et al 1994), wasps (O'Donnell 1998), and in a few ant species (Stuart & Page 1991;Hughes et al 2003). Similarly, a significant genetic component to division of labour has been reported in ant colonies headed by multiple queens (polygyny), with workers belonging to different matrilines showing a different propensity to perform distinct tasks (Snyder 1992;Blatrix et al 2000;Julian et al 2002).…”