The Antennal Lobes of Fungus-Growing Ants (Attini): Neuroanatomical Traits and Evolutionary Trends

Abstract

Ants of the tribe Attini are characterized by their obligate cultivation of symbiotic fungi. In addition to the complex chemical communication system of ants in general, substrate selection and fungus cultivation pose high demands on the olfactory system of the Attini. Indeed, behavioral studies have shown a rich diversity of olfactory-guided behaviors and tremendous odor sensitivity has been demonstrated. To allow fine-tuned behavioral responses, adaptations within the olfactory system of the Attini are expected. We compared the number, volumes and position of the glomeruli (functional units) of the antennal lobe of 25 different species from all three major Attini groups (lower, higher and leaf-cutting Attini). The antennal lobes of all investigated Attini comprise a high number of glomeruli (>257). The highest number (630) was found in Apterostigma cf. mayri. This species is at a basal position within the Attini phylogeny, and we suggest that a high number of glomeruli might have been advantageous in the evolution of the advanced olfactory systems of the Attini. In the leaf-cutting Attini, an extremely large glomerulus (macroglomerulus) near the antennal nerve entrance was recently described in two species. Preliminary results show that this macroglomerulus is involved in processing of trail-pheromone information. In our comparative study, we find this macroglomerulus in all investigated leaf-cutting Attini, but in none of the lower and higher Attini species. It is found only in large workers, and for all investigated species it is located close to the entrance of the antennal nerve. Our results indicate that the presence of a macroglomerulus in large workers of leaf-cutting Attini is a derived over-expression of a trait in the polymorphic leaf-cutting species. It presumably represents an olfactory adaptation to elaborate foraging and mass recruitment systems, and adds to the complexity of division of labor and social organization known for this group.

Evolution of brain elaboration

“…Further adaptations of the primary olfactory system also take a similar form across phyla: both insects and vertebrate species that rely heavily on olfaction have larger arrays of functional olfactory receptor genes in the genome [19 -21] and larger olfactory bulbs/antennal lobes with more glomeruli [22][23][24][25]. Interestingly, these structures do not appear to be capable of adapting to a return to an aquatic lifestyle, as olfactory bulbs and antennal lobes are lost or greatly reduced in secondarily aquatic animals such as cetaceans or whirligig beetles [26,27].…”

Antennal-Lobe Organization in Desert Ants of the Genus Cataglyphis

“…Glands and tracheae were gently removed, and the brains were dissected and fixed immediately in ice-cold Fix-Mix (2% paraformaldehyde/2% glutaraldehyde) in phosphate-buffered saline (PBS, pH 7.2) and stored for 3-30 days in the fridge. This fixation leads to increased autofluorescence which, compared to formaldehyde fixation only, allowed us to better identify the outlines of glomeruli [Kelber et al, 2009]. The brains were then rinsed in PBS (3 !…”

“…Therefore, the median (all data were not normally distributed: KolmogorovSmirnov procedure, p ! 0.05) of all glomerular volumes was calculated for each AL to subsequently compute the ratio of the volume of each glomerulus and the median volume (method modified after Kelber et al [2009]). This normalized volume describes how many times bigger a single glomerulus is compared to the median size of all glomeruli.…”

“…In several insect species, sex-pheromone-sensitive ORNs in males of moths [Anton and Homberg, 1999] or honeybee drones [Arnold et al, 1985;Sandoz, 2006], for example, send their projections to a single or to several enlarged glomeruli, the so-called macroglomeruli (MGs) or MG complexes (MGCs). In non-sexual individuals of leaf-cutting ants (Atta and Acromyrmex), an MG was found in large workers [Kleineidam et al, 2005;Kelber et al, 2009], where it is involved in the detection and processing of trail pheromone components [Kuebler et al, 2010].…”

Investment in higher order central processing regions is not constrained by brain size in social insects

“…Even less attention has been given to the scaling of the major primary sensory input neuropils-the antennal (AL) and optic lobes (OL)-which process olfactory and visual afferent information, respectively, and supply the mushroom body calyces (C) in hymenopterans. Understanding how these aspects of brain composition affect worker behaviour and division of labour has been a prominent goal of social insect research, and significant interspecific variation in brain composition associated with task performance has begun to be identified in ants [21,33,47,50] and wasps [51]. Absolute brain size was recently proposed to constrain the evolution of the organization of the functional module comprising the C, AL and OL in polistine wasps [49]; interspecific comparisons suggested that small-brained wasps have lower ratios of C volume to the combined volume of the AL þ OL (C/AO hereafter) owing to positive allometry between C and brain size and negative allometry between AL þ OL and brain size.…”