Discussion
As hypothesized, sexual dimorphism covaries with worker polymorphism.
This pattern is evident when comparing the size-shape space of
individual species as well as at the level of entire genera. While quite
logical, that male and female characters do not evolve independently,
even in the absence of sexual selection, males have largely been absent
from empirical and theoretical studies of the hymenopteran social insect
castes.
While this study documents how sexual dimorphism relates to worker
polymorphism in two genera of highly social and very derived ants, it is
logical to think that sexual dimorphism was important for the origin of
the worker caste and all of its subsequent elaboration/modification.
Because sexual dimorphism is likely the ancestral state of the
Hymenoptera (Stubblefield and Seger 1994), the ancestral size-shape
space in the wasp ancestor of the ants was the phenotype space available
for selection that ultimately resulted in the worker caste. After all,
the differences among castes is primarily the difference in the timing,
location, and dosage of a shared set of genes, and so the worker was/is
both part male and part female. Variation in mating and social systems
among ant species varies the degree of sexual selection and thus sexual
dimorphism. Thus it is likely that there is a correlation between mating
systems and worker polymorphism. It may even be that the observed
correlation between worker caste variation and genetic diversity within
nests (Fjerdingstad and Crozier 2006, Anderson et al. 2008, Smith et al.
2008b, Hughes and Boomsma 2008, Smith et al. 2008a), that results from
mating systems like polyandry, is mechanistically confounded by the
phenotypic results of sexual selection (e.g., sexual, or natural,
selection on male body size to increase mating probability).
The causal arrow in the relationship between sexual and worker
dimorphism likely points in both directions. As above, sexual dimorphism
may have provided the raw material (size-shape) for the evolution of the
worker caste, but selection on worker characteristics, and on the
population of workers in colonies (colony-level selection)(Oster and
Wilson 1979), likely facilitates/inhibits the phenotypic variation
available to sexual selection. Strong natural selection on worker size
variation, for example, increases the size-shape space and may
facilitate the production of novel sexual forms.
Importantly, the causal direction of the relationship is far less
important than recognizing the non-independence of the two processes.
Selection on worker polymorphism, for example, increases the phenotypic
space available to sexual selection, not necessarily whether that
selection occurs. Selection for increased variation in the size-shape of
any caste increases the raw material for selection – it increases
opportunity. As previously theorized, the colony environment buffers its
members from individual-level selection and can be an incubator of sorts
for novelty, especially via modifications of the social environment
(Rajakumar et al. 2012, Molet et al. 2012).
Not surprisingly, queen-worker dimorphism was a better predictor of
worker polymorphism than was sexual dimorphism because female castes are
developmentally more similar than are the sexes. Previous studies have
documented the correlation between queen-worker and worker polymorphism
across species (Fjerdingstad and Crozier 2006), though these factors are
not always correlated (Lecocq de Pletincx et al. 2021). The development
of workers and queens is more similar than that of workers and males
(Anderson et al. 2008). For example, queen-worker differentiation takes
place in early development while worker caste differentiation occurs
later; note, the most upstream mechanisms of female caste determination
can occur prior to fertilization or in early embryogenesis (Schwander et
al. 2008), but most differentiation (Lillico-Ouachour and Abouheif
2017), and canalization (Qiu et al. 2022), occurs later in larval
development. Hymenopteran males and females differ genetically where
male-destined eggs are typically unfertilized, and at least in honeybees
the mechanism involves heterozygosity at a single locus, CSD, that then
feeds into the conserved sex differentiation pathway of insects (Beye et
al. 2003, Roth et al. 2019). Many studies are now demonstrating that
sexual determination and differentiation and caste determination and
differentiation are not mechanistically independent, both pathways
utilize many of the same genes (Klein et al. 2016, Johnson and Jasper
2016, Warner et al. 2019, Roth et al. 2019).
One of the most surprising results of this study is the size-shape axis
in both Pogonomyrmex species. In P. barbatus there is a
size-shape relationship among workers, and in P. badius this
relationship is the axis that differentiates both worker castes and both
sexes (though workers and sexuals have different intercepts). The major
worker caste in P. badius is an evolutionary novelty in the sense
that it is a unique and derived character for the species, completely
absent in all other extant North American Pogonomyrmex . Based on
the measurements taken, the major worker is simply an extension of the
minor worker along the size-shape axis. The major caste, in other words,
is simply a size increase of the minor worker using the same allometric
growth rules – and the gyne is, in a sense, a size extension of the
male using the same allometic growth rules – and surprisingly, workers
and sexuals vary on parallel axes only differing in their starting size.
This result suggests that, despite appearances, all castes differ only
slightly in basic developmental scaling.
Clearly, including more genera and more body measurements is a logical
next step to further evaluate the relationship between sexual dimorphism
and worker polymorphism. Looking at more subfamilies of ant will likely
also reveal how generalizable this pattern is and how other aspects of
biology constrain or facilitate caste evolution. Fortunately, the
growing database of Antweb.org is an amazing resource and it seems that
the maintainers of the database have done a commendable job of
representing species-level variation. Given the high quality and
taxonomic breadth of the database it is sure that it will be useful for
the evaluation of additional macroevolutionary patterns in ants.
Additionally, the availability of three-dimensional data for ant
morphology and anatomy promises to add significantly to our knowledge of
how castes differ in complex elements of internal anatomy and shape.