INTRODUCTION
Nutrition is an upstream organizer of most organismal processes, and
thus dealing with variation in the availability of nutrients is among
the most consequential challenges, and selective agents, faced by all
organisms (Stearns, 1992; Zera & Harshman, 2001). While many nutrients
are necessary for maintenance and growth, the majority consumed and used
are macronutrients ingested in high quantity, such as proteins,
carbohydrates, and fats (Raubenheimer, Simpson, & Mayntz, 2009). The
molecular mechanisms that translate incoming macronutrients into
maintenance, new tissue, or storage, are well understood, and tend to be
highly conserved (Conlon & Raff, 1999).
Superorganisms, like eusocial insects, are groups of individuals of the
same species operating in a synergistic way (D. S. Wilson & Sober,
1989). Superorganisms are characterized by the reproductive division of
labour, such that some individuals do not reproduce (somatic – germ
line division) (Hölldobler & Wilson, 2009). The nutritional challenges
of any cell or organism are also faced by superorganisms, but are
compounded by the additional level of complexity (cooperating organisms
on top of cooperating cells, etc.) – the labour that is divided amongst
cells in ‘unitary’ organisms is divided amongst individuals in
the superorganism. How, then, do nutritional challenges scale from
organism to superorganism? Do organism and superorganism have different
nutritional optima and/or face the same nutrition-mediated trade-offs?
If individual and superorganism optima are not aligned, then processes
occurring at the individual level may limit those at the superorganismal
level.
Social insect colonies undergo a coordinated development that is
responsive to the environment and also lineage/species specific, termed
‘sociogenesis’ (E. O. Wilson, 1985). ‘Sociometry’ is a general term
applied to the metrics associated with superorganisms, such as colony
size, individual size (and size distributions), the numbers and ratios
of different castes, among others. As a general pattern in studies of
sociometry and sociogenesis, worker size increases with the number of
workers in the colony (Smith & Tschinkel, 2006; Tschinkel, 1987, 1993,
1998). This relationship is at least in part due to increasing resource
availability to developing individuals in larger colonies - increased
nutrient availability does increase worker production and worker size
(Goetsch, 1937; Metzl, Wheeler, & Abouheif, 2018; Passera, 1974; Smith,
2007; Wills et al., 2015). Increased protein/nitrogen content has also
been associated with the production of larger workers (majors/soldiers)
and sexual castes (Bono & Heithaus, 2002; Goetsch, 1937; Hunt &
Nalepa, 1994; Passera, 1974; Schmidt, Hunt, & Smith, 2012; Smith,
Anderson, Tillberg, Gadau, & Suarez, 2008; Smith & Suarez, 2010;
Smith, 1942). However, previous studies have been largely observational
or used natural foods (e.g., increased insect prey) that confound
protein/nitrogen content with many other nutrient
differences. Furthermore, many previous studies focus on short-term
colony dynamics, documenting adult worker survival rather than
longer-term growth (e.g., Dussutour & Simpson, 2009, 2012; Wills et
al., 2015).
The nutritional basis of individual and superorganism size is a major
unresolved issue in the understanding of social insect growth and
development. In the present study, we used ants as a model superorganism
and employed a nutritional geometry framework (Simpson & Raubenheimer,
1995) that allowed for the manipulation of both the ratio and amounts of
protein and carbohydrate available to colonies. We hypothesized
that worker size and colony size would both increase with increasing
availability of protein in the diet – that is, worker number and size
are both protein-limited. This hypothesis is consistent with sociometric
observations. An important alternative hypothesis is that worker and
colony development are limited by different nutrients (i.e., worker and
colony optima differ). For example, worker size may indeed be
protein-limited, but colonies may be more carbohydrate limited due to
the metabolic demands of the standing crop of adult workers. This
alternative hypothesis is premised on there being a nutritionally
mediated life-history trade-off between growth (new tissue)
and maintenance (current tissue, Fig. 1).
A division of labour inherent in social insect colonies is between
growing individuals (larvae) and those that maintain the colony
(workers). To further explore possible trade-offs between growth and
maintenance, we examined the flow of nutrients through these two types
of individual, larva and worker, using a stable isotope tracer
experiment. We hypothesized that protein would be more rapidly and
completely transferred to larvae while carbohydrates would persist
longer in workers.
Lastly, we examined natural (field) colony preference for macronutrient
ratios to test whether preference matched the nutrient ratios that
maximized growth in the lab. We hypothesized that colonies would prefer
what maximized lab growth. However, an alternative hypothesis is that
worker preference is not aligned with colony growth (under lab
conditions), but instead is more tuned to the adult worker optimum of
high carbohydrates – this may be selectively advantageous by favouring
colony maintenance over growth. Furthermore, workers are the collectors
of the food and preferences based on their own physiology and current
state build from the ancestral condition of solitary insects. Other
alternative hypotheses include that colonies respond based on experience
or environmental variation, among other factors.