Insect PRXamides: Evolutionary Divergence, Novelty, and Loss in a Conserved Neuropeptide System.

The PRXamide neuropeptides have been described in both protostome and deuterostome species, including all major groups of the Panarthropoda. Best studied are the insect PRXamides consisting of three genes: pk/pban, capa, and eth, each encoding multiple short peptides that are cleaved post-translationally. Comparisons of genome and transcriptome sequences reveal that while retaining its fundamental ancestral organization, the products of the pk/pban gene have undergone significant change in the insect Order Diptera.

The rise to dominance of genetic model organisms and the decline of curiosity-driven organismal research.

Curiosity-driven, basic biological research "…performed without thought of practical ends…" establishes fundamental conceptual frameworks for future technological and medical breakthroughs. Traditionally, curiosity-driven research in biological sciences has utilized experimental organisms chosen for their tractability and suitability for studying the question of interest. This approach leverages the diversity of life to uncover working solutions (adaptations) to problems encountered by living things, and evolutionary context as to the extent to which these solutions may be generalized to other species.

Insect societies and the social brain.

The 'social brain hypothesis,' the relationship between social behavior and brain size, does not apply to insects. In social insects, especially those of the Order Hymenoptera (ants, bees and wasps), sociality has not always increased individual behavioral repertoires and is associated with only subtle variation in the size of a higher brain center, the mushroom bodies. Rather than sociality, selection for novel visual behavior, perhaps spatial learning, has led to the acquisition of novel visual inputs and profound increases in mushroom body size.

Evolution of brain elaboration.

Large, complex brains have evolved independently in several lineages of protostomes and deuterostomes. Sensory centres in the brain increase in size and complexity in proportion to the importance of a particular sensory modality, yet often share circuit architecture because of constraints in processing sensory inputs. The selective pressures driving enlargement of higher, integrative brain centres has been more difficult to determine, and may differ across taxa.

Evolution of complex higher brain centers and behaviors: behavioral correlates of mushroom body elaboration in insects.

Large, complex higher brain centers have evolved many times independently within the vertebrates, but the selective pressures driving these acquisitions have been difficult to pinpoint. It is well established that sensory brain centers become larger and more structurally complex to accommodate processing of a particularly important sensory modality. When higher brain centers such as the cerebral cortex become greatly expanded in a particular lineage, it is likely to support the coordination and execution of more complex behaviors, such as those that require flexibility, learning, and social interaction, in response to selective pressures that made these new behaviors advantageous.

Miniaturization of nervous systems and neurons.

Miniaturized species have evolved in many animal lineages, including insects and vertebrates. Consequently, their nervous systems are constrained to fit within tiny volumes. These miniaturized nervous systems face two major challenges for information processing: noise and energy consumption.

Are mushroom bodies cerebellum-like structures?

The mushroom bodies are distinctive neuropils in the protocerebral brain segments of many protostomes. A defining feature of mushroom bodies is their intrinsic neurons, masses of cytoplasm-poor globuli cells that form a system of lobes with their densely-packed, parallel-projecting axon-like processes. In insects, the role of the mushroom bodies in olfactory processing and associative learning and memory has been studied in depth, but several lines of evidence suggest that the function of these higher brain centers cannot be restricted to these roles.

Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects.

The social brain hypothesis posits that the cognitive demands of social behaviour have driven evolutionary expansions in brain size in some vertebrate lineages. In insects, higher brain centres called mushroom bodies are enlarged and morphologically elaborate (having doubled, invaginated and subcompartmentalized calyces that receive visual input) in social species such as the ants, bees and wasps of the aculeate Hymenoptera, suggesting that the social brain hypothesis may also apply to invertebrate animals. In a quantitative and qualitative survey of mushroom body morphology across the Hymenoptera, we demonstrate that large, elaborate mushroom bodies arose concurrent with the acquisition of a parasitoid mode of life at the base of the Euhymenopteran (Orussioidea + Apocrita) lineage, approximately 90 Myr before the evolution of sociality in the Aculeata.

A subpopulation of mushroom body intrinsic neurons is generated by protocerebral neuroblasts in the tobacco hornworm moth, Manduca sexta (Sphingidae, Lepidoptera).

Subpopulations of Kenyon cells, the intrinsic neurons of the insect mushroom bodies, are typically sequentially generated by dedicated neuroblasts that begin proliferating during embryogenesis. When present, Class III Kenyon cells are thought to be the first born population of neurons by virtue of the location of their cell somata, farthest from the position of the mushroom body neuroblasts. In the adult tobacco hornworm moth Manduca sexta, the axons of Class III Kenyon cells form a separate Y tract and dorsal and ventral lobelet; surprisingly, these distinctive structures are absent from the larval Manduca mushroom bodies.

Ground plan of the insect mushroom body: functional and evolutionary implications.

In most insects with olfactory glomeruli, each side of the brain possesses a mushroom body equipped with calyces supplied by olfactory projection neurons. Kenyon cells providing dendrites to the calyces supply a pedunculus and lobes divided into subdivisions supplying outputs to other brain areas. It is with reference to these components that most functional studies are interpreted.

Evolutionary convergence of higher brain centers spanning the protostome-deuterostome boundary.

Currently available evidence supports a single origin for the centralized nervous system of bilaterally symmetrical animals. Beneath the staggering diversity of protostome and deuterostome nervous systems lies a fundamental groundplan consisting of a tripartite brain and a nerve cord divided into distinct antero-posterior and medio-lateral zones. As divergent lineages have taken independent paths towards increased encephalization, complex brain centers have arisen that serve multiple levels of sensory processing and advanced behavioral coordination and execution.

Tritocerebral tract input to the insect mushroom bodies.

Insect mushroom bodies, best known for their role in olfactory processing, also receive sensory input from other modalities. In crickets and grasshoppers, a tritocerebral tract containing afferents from palp mechanosensory and gustatory centers innervates the accessory calyx. The accessory calyx is uniquely composed of Class III Kenyon cells, and was shown by immunohistochemistry to be present sporadically across several insect orders.

Structural, functional and developmental convergence of the insect mushroom bodies with higher brain centers of vertebrates.

Convergence of higher processing centers has been proposed for insects and vertebrates, but the extent of these similarities remains controversial. The present study demonstrates that one higher brain center of insects, the mushroom bodies, displays a number of similarities with mammalian higher brain centers that are arguably the products of adaptation to common behavioral ecologies, despite their deeply divergent origins. Quantitative neuroanatomy, immunohistochemistry, fluorescent tract tracing and BrdU labeling are employed to investigate the relationships among behavioral ecology and mushroom body size, sensory input and mode of development in one taxon, the scarab beetles (Coleoptera: Scarabaeidae).

Development and evolution of the insect mushroom bodies: towards the understanding of conserved developmental mechanisms in a higher brain center.

The insect mushroom bodies are prominent higher order neuropils consisting of thousands of approximately parallel projecting intrinsic neurons arising from the minute basophilic perikarya of globuli cells. Early studies described these structures as centers for intelligence and other higher functions; at present, the mushroom bodies are regarded as important models for the neural basis of learning and memory. The insect mushroom bodies share a similar general morphology, and the same basic sequence of developmental events is observed across a wide range of insect taxa.

Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects.

Here we demonstrate the independent acquisition of strikingly similar brain architectures across divergent insect taxa and even across phyla under similar adaptive pressures. Convoluted cortical gyri-like structures characterize the mushroom body calyces in the brains of certain species of insects; we have investigated in detail the cellular and ecological correlates of this morphology in the Scarabaeidae (scarab beetles). "Gyrencephalic" mushroom bodies with increased surface area and volume of calycal synaptic neuropils and increased intrinsic neuron number characterize only those species belonging to generalist plant-feeding subfamilies, whereas significantly smaller "lissencephalic" mushroom bodies are found in more specialist dung-feeding scarab beetles.

Developmental organization of the mushroom bodies of Thermobia domestica (Zygentoma, Lepismatidae): insights into mushroom body evolution from a basal insect.

The mushroom bodies of the insect brain are sensory integration centers best studied for their role in learning and memory. Studies of mushroom body structure and development in neopteran insects have revealed conserved morphogenetic mechanisms. The sequential production of morphologically distinct intrinsic neuron (Kenyon cell) subpopulations by mushroom body neuroblasts and the integration of newborn neurons via a discrete ingrowth tract results in an age-based organization of modular subunits in the primary output neuropil of the mushroom bodies, the lobes.

Development and morphology of class II Kenyon cells in the mushroom bodies of the honey bee, Apis mellifera.

Class II Kenyon cells, defined by their early birthdate and unique dendritic arborizations, have been observed in the mushroom bodies of evolutionarily divergent insects. In the fruit fly Drosophila melanogaster, Class II (also called clawed) Kenyon cells are well known for their extensive reorganization that occurs during metamorphosis. The present account reports for the first time the occurrence of mushroom body reorganization during metamorphosis in holometabolous insect species outside of the Diptera.

Limits on volume changes in the mushroom bodies of the honey bee brain.

The behavioral maturation of adult worker honey bees is influenced by a rising titer of juvenile hormone (JH), and is temporally correlated with an increase in the volume of the neuropil of the mushroom bodies, a brain region involved in learning and memory. We explored the stability of this neuropil expansion and its possible dependence on JH. We studied the volume of the mushroom bodies in adult bees deprived of JH by surgical removal of the source glands, the corpora allata.

A unique mushroom body substructure common to basal cockroaches and to termites.

The mushroom bodies of the cockroach Periplaneta americana are made up of intrinsic neurons (class I and class II Kenyon cells) with dendrites in a dorsal calyx and axons that bifurcate into medial and vertical lobes. Here, we describe a substructure of the cockroach mushroom bodies composed of a previously unrecognized class of Kenyon cells with distinct morphologies. The embryonically produced class III Kenyon cells form a separate accessory calyx below the calyx proper.