Introduction
Male ants are ephemeral in the annual cycle of a colony. They have been
likened to ‘sperm missiles’ (a statement attributed to E. O. Wilson) –
a transient, but essential function – delivering the male gametes of
the superorganism to gynes so that the gynes can become queens and found
new colonies, beginning the colonial life cycle anew (Hölldobler et al.
1990). Because of this males are often unseen and unsampled. Males are
also haploid, typically developing from unfertilized eggs (males can be
fathers, but have no father). Males are thus genetically and
behaviorally very very different from the standard (female) ant, and
their morphology is also clearly distinct as they typically have small
heads with big eyes, a large muscly thorax with wings, and an abdomen
tipped with an intromittent organ rather than a stinger. They are very
clearly different than females; so different to look a different species
(Fig. 1). And so it is clear why males are largely ignored in the
empirical and theoretical literature on caste and polyphenism in the
social insects – they are different.
Recent studies on gene expression during development have revealed that
queen-worker caste determination shares many genes in common with
male-female sex determination (Klein et al. 2016, Johnson and Jasper
2016, McAfee et al. 2019, Warner et al. 2019, Roth et al. 2019). In
fact, in both an ant and honeybee there was a large suite of shared gene
expression patterns between males and workers to the exclusion of gynes
(Warner et al. 2019). Furthermore, in a CRISPR gene knockout of early
sex determination genes in honeybee it was shown that the Fem(feminizer) gene appears to control gonad size regardless of sex (though
it also interacts with sex determination)(Roth et al. 2019). The
emerging picture is that worker caste differentiation (from queens)
arose via the co-option of male genes. That is, workers might be a
gene-expression developmental mosaic (Molet et al. 2012) of male and
female.
The view that male-ness contributed (and contributes) to worker
evolution is logical. Male and female ants, despite behavioral, genetic,
and morphological dissimilarity, arise from the same genome, whether
haploid or diploid. Thus the raw material for natural selection to work
from is the combination of phenotype expressed by both males and
females; the colonial lifestyle of social insects may also buffer novel
developmental mosaics from strong selection (Molet et al. 2012). Sexual
dimorphism is present in most clades of Hymenoptera at least partly
because of specialization by females for parasitism/predation and brood
care (in some lineages)(Stubblefield and Seger 1994). Due to sexual
dimorphism there was morphological variation for selection to act on –
possibly enough to recombine developmental programs and produce a novel
phenotype/caste that changed ecological and evolutionary history (Smith
and Szathmary 1997), the worker. In this study I examine whether there
is evidence for sexual dimorphism explaining variation in worker caste
polymorphism. In extant species, does the degree of sexual dimorphism
correlate with how variable the worker caste is – in other words, does
male-ness have a hand in the evolution and elaboration of the worker
caste?
Two species of Pogonomyrmex harvester ant, P. barbatus andP. badius , were used to examine the relationship between ant size
and shape across all adult castes. These species were chosen because
sufficient samples were available across all castes for detailed
measurement and because they differ in regard to both sexual and worker
dimorphism. P. barbatus has very little sexual dimorphism while
in P. badius , gynes are more than three times the size of males
by dry mass and have an energetic cost to the colony of 4.5X of a male
(Smith and Tschinkel 2006). Similarly, workers of P. barbatus are
characterized as monomorphic while those of P. badius are
dimorphic, with clearly distinct major and minor worker sub-castes
(Tschinkel 1998).