RESUMEN
Hymenoptera possess voluminous mushroom bodies (MBs), brain centres associated with sensory integration, learning and memory. The mushroom body input region (calyx) is organized in distinct synaptic complexes (microglomeruli, MG) that can be quantified to analyse body size-related phenotypic plasticity of synaptic microcircuits in these small brains. Leaf-cutting ant workers (Atta vollenweideri) exhibit an enormous size polymorphism, which makes them outstanding to investigate neuronal adaptations underlying division of labour and brain miniaturization. We particularly asked how size-related division of labour in polymorphic workers is reflected in volume and total numbers of MG in olfactory calyx subregions. Whole brains of mini, media and large workers were immunolabelled with anti-synapsin antibodies, and mushroom body volumes as well as densities and absolute numbers of MG were determined by confocal imaging and three-dimensional analyses. The total brain volume and absolute volumes of olfactory mushroom body subdivisions were positively correlated with head widths, but mini workers had significantly larger MB to total brain ratios. Interestingly, the density of olfactory MG was remarkably independent from worker size. Consequently, absolute numbers of olfactory MG still were approximately three times higher in large compared with mini workers. The results show that the maximum packing density of synaptic microcircuits may represent a species-specific limit to brain miniaturization.
Asunto(s)
Hormigas/anatomía & histología , Hormigas/fisiología , Animales , Hormigas/genética , Encéfalo/anatomía & histología , Encéfalo/fisiología , Cuerpos Pedunculados/fisiología , Percepción Olfatoria , Sinapsis/fisiologíaRESUMEN
The antennae of honeybee (Apis mellifera) workers and drones differ in various aspects. One striking difference is the presence of Sensilla basiconica in (female) workers and their absence in (male) drones. We investigate the axonal projection patterns of olfactory receptor neurons (ORNs) housed in S. basiconica in honeybee workers by using selective anterograde labeling with fluorescent tracers and confocal-microscopy analysis of axonal projections in antennal lobe glomeruli. Axons of S. basiconica-associated ORNs preferentially projected into a specific glomerular cluster in the antennal lobe, namely the sensory input-tract three (T3) cluster. T3-associated glomeruli had previously been shown to be innervated by uniglomerular projection (output) neurons of the medial antennal lobe tract (mALT). As the number of T3 glomeruli is reduced in drones, we wished to determine whether this was associated with the reduction of glomeruli innervated by medial-tract projection neurons. We retrogradely traced mALT projection neurons in drones and counted the innervated glomeruli. The number of mALT-associated glomeruli was strongly reduced in drones compared with workers. The preferential projections of S. basiconica-associated ORNs in T3 glomeruli together with the reduction of mALT-associated glomeruli support the presence of a female (worker)-specific olfactory subsystem that is partly innervated by ORNs from S. basiconica and is associated with the T3 cluster of glomeruli and mALT projection neurons. We propose that this olfactory subsystem supports parallel olfactory processing related to worker-specific olfactory tasks such as the coding of colony odors, colony pheromones and/or odorants associated with foraging on floral resources.
Asunto(s)
Vías Olfatorias/fisiología , Sensación/fisiología , Caracteres Sexuales , Animales , Antenas de Artrópodos/citología , Antenas de Artrópodos/inervación , Axones/fisiología , Abejas , Femenino , Masculino , Modelos Biológicos , Neuronas Receptoras Olfatorias/fisiología , Coloración y EtiquetadoRESUMEN
Sexually dimorphic sensory systems are common in Hymenoptera and are considered to result from sex-specific selection pressures. An extreme example of sensory dimorphism is found in the solitary bee tribe Eucerini. Males of long-horned bees bear antennae that exceed body length. This study investigated the pronounced sexual dimorphism of the peripheral olfactory system and its representation in higher brain centers of the species Eucera berlandi. Eucera males have elongated antennae, with 10 times more pore plates and three times more olfactory receptor neurons than females. The male antennal lobe (AL) comprises fewer glomeruli than the female AL (â¼100 vs. â¼130), of which four are male-specific macroglomeruli. No sex differences were found in the relative volume of the mushroom bodies, a higher order neuropil essential for learning and memory in Hymenoptera. Compared with the Western honeybee, the degree of sexual dimorphism in Eucera is more pronounced at the periphery. In contrast, sex differences in glomerular numbers are higher in the eusocial honeybee and a sexual dimorphism of the relative investment in mushroom body tissue is observed only in Apis. The observed differences between the eusocial and the solitary bee species may reflect differences in male-specific behavioral traits and associated selection pressures, which are discussed in brief.
Asunto(s)
Abejas/anatomía & histología , Neuronas/fisiología , Vías Olfatorias/anatomía & histología , Vías Olfatorias/fisiología , Caracteres Sexuales , Adaptación Fisiológica , Animales , Abejas/clasificación , Femenino , Masculino , Neurópilo/fisiología , Especificidad de la EspecieRESUMEN
Desert ants of the genus Cataglyphis possess remarkable visual navigation capabilities. Although Cataglyphis species lack a trail pheromone system, Cataglyphis fortis employs olfactory cues for detecting nest and food sites. To investigate potential adaptations in primary olfactory centers of the brain of C. fortis, we analyzed olfactory glomeruli (odor processing units) in their antennal lobes and compared them to glomeruli in different Cataglyphis species. Using confocal imaging and 3D reconstruction, we analyzed the number, size and spatial arrangement of olfactory glomeruli in C. fortis, C.albicans, C.bicolor, C.rubra, and C.noda. Workers of all Cataglyphis species have smaller numbers of glomeruli (198-249) compared to those previously found in olfactory-guided ants. Analyses in 2 species of Formica - a genus closely related to Cataglyphis - revealed substantially higher numbers of olfactory glomeruli (c. 370), which is likely to reflect the importance of olfaction in these wood ant species. Comparisons between Cataglyphis species revealed 2 special features in C. fortis. First, with c. 198 C. fortis has the lowest number of glomeruli compared to all other species. Second, a conspicuously enlarged glomerulus is located close to the antennal nerve entrance. Males of C. fortis possess a significantly smaller number of glomeruli (c. 150) compared to female workers and queens. A prominent male-specific macroglomerulus likely to be involved in sex pheromone communication occupies a position different from that of the enlarged glomerulus in females. The behavioral significance of the enlarged glomerulus in female workers remains elusive. The fact that C. fortis inhabits microhabitats (salt pans) that are avoided by all other Cataglyphis species suggests that extreme ecological conditions may not only have resulted in adaptations of visual capabilities, but also in specializations of the olfactory system.
Asunto(s)
Hormigas/anatomía & histología , Antenas de Artrópodos/inervación , Ganglios de Invertebrados/anatomía & histología , Bulbo Olfatorio/anatomía & histología , Vías Olfatorias/anatomía & histología , Adaptación Biológica , Animales , Femenino , Masculino , Factores Sexuales , Especificidad de la EspecieRESUMEN
In the leaf-cutting ant Atta vollenweideri, the worker caste exhibits a pronounced size-polymorphism, and division of labor is dependent on worker size (alloethism). Behavior is largely guided by olfaction, and the olfactory system is highly developed. In a recent study, two different phenotypes of the antennal lobe of Atta vollenweideri workers were found: MG- and RG-phenotype (with/without a macroglomerulus). Here we ask whether the glomerular numbers are related to worker size. We found that the antennal lobes of small workers contain approximately 390 glomeruli (low-number; LN-phenotype), and in large workers we found a substantially higher number of approximately 440 glomeruli (high-number; HN-phenotype). All LN-phenotype workers and some small HN-phenotype workers do not possess an MG (LN-RG-phenotype and HN-RG-phenotype), and the remaining majority of HN-phenotype workers do possess an MG (HN-MG-phenotype). Using mass-staining of antennal olfactory receptor neurons we found that the sensory tracts divide the antennal lobe into six clusters of glomeruli (T1-T6). In LN-phenotype workers, approximately 50 glomeruli are missing in the T4-cluster. Selective staining of single sensilla and their associated receptor neurons revealed that T4-glomeruli are innervated by receptor neurons from the main type of olfactory sensilla, the Sensilla trichodea curvata. The other type of olfactory sensilla (Sensilla basiconica) exclusively innervates T6-glomeruli. Quantitative analyses of differently sized workers revealed that the volume of T6 glomeruli scales with the power of 2.54 to the number of Sensilla basiconica. The results suggest that developmental plasticity leading to antennal-lobe phenotypes promotes differences in olfactory-guided behavior and may underlie task specialization within ant colonies.
Asunto(s)
Hormigas/citología , Células Receptoras Sensoriales/citología , Conducta Social , Animales , Hormigas/anatomía & histología , Axones , Encéfalo/anatomía & histología , Encéfalo/citología , Recuento de Células , Imagenología Tridimensional , Microscopía Confocal , Plasticidad Neuronal , Vías Olfatorias/anatomía & histología , Vías Olfatorias/citología , Neuronas Receptoras Olfatorias/citología , Tamaño de los Órganos , FenotipoRESUMEN
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.
Asunto(s)
Hormigas/anatomía & histología , Encéfalo/anatomía & histología , Vías Olfatorias/anatomía & histología , Animales , Hormigas/microbiología , Hormigas/fisiología , Conducta Alimentaria , Hongos/fisiología , Procesamiento de Imagen Asistido por Computador , Microscopía Confocal , Neuronas Receptoras Olfatorias/anatomía & histología , Tamaño de los Órganos , Especificidad de la Especie , SimbiosisRESUMEN
The poreplate sensilla of honeybees are equipped with multiple olfactory receptor neurons (ORNs), which innervate glomeruli of the antennal lobe (AL). We investigated the axonal projection pattern in glomeruli of the AL (glomerular pattern), formed by the multiple ORNs of individual poreplate sensilla. We used the different glomerular patterns to draw conclusions about the equipment of poreplate sensilla with different ORN types. ORNs of single poreplate sensilla were stained and analyzed by laser-scanning confocal microscopy and 3D software (AMIRA). In 13 specimens we found between 7 and 23 ORNs. This is in accordance with data found in the literature (5-35 ORNs) suggesting that all ORNs of the single poreplate sensilla were stained. The ORNs innervate the AL via all four sensory tracts (T1-T4), and glomeruli of the anterior part of the AL are more often innervated. Each ORN innervates a single glomerulus (uniglomerular), and all ORNs of one poreplate sensillum project to different glomeruli. Visual inspection and individual identification of glomeruli, based on the honeybee digital AL atlas, were used to evaluate mapping of glomeruli by a rigid transformation of the experimental ALs onto a reference AL. ORNs belonging to individual poreplate sensilla form variable glomerular patterns, and we did not find a common organization of glomerular patterns. We conclude that poreplate sensilla are equipped with different ORN types but that the same ORN types can be found in different poreplate sensilla. The equipment of poreplate sensilla with ORNs is overlapping. The mapping of glomeruli by rigid transformation is revealed to be a powerful tool for comparative neuroanatomy.