An official website of the United States government
Descriptions of crustacean brains have focused mainly on three highly derived lineages of malacostracans: the reptantian infraorders represented by spiny lobsters, lobsters, and crayfish. Those descriptions advocate the view that dome- or cap-like neuropils, referred to as ‘hemiellipsoid bodies,’ are the ground pattern organization of centers that are comparable to insect mushroom bodies in processing olfactory information. Here we challenge the doctrine that hemiellipsoid bodies are a derived trait of crustaceans, whereas mushroom bodies are a derived trait of hexapods. We demonstrate that mushroom bodies typify lineages that arose before Reptantia and exist in Reptantia thereby indicating that the mushroom body, not the hemiellipsoid body, provides the ground pattern for both crustaceans and hexapods. We show that evolved variations of the mushroom body ground pattern are, in some lineages, defined by extreme diminution or loss and, in others, by the incorporation of mushroom body circuits into lobeless centers. Such transformations are ascribed to modifications of the columnar organization of mushroom body lobes that, as shown in Drosophila and other hexapods, contain networks essential for learning and memory.
more »
« less
Shore crabs reveal novel evolutionary attributes of the mushroom body
Neural organization of mushroom bodies is largely consistent across insects, whereas the ancestral ground pattern diverges broadly across crustacean lineages resulting in successive loss of columns and the acquisition of domed centers retaining ancestral Hebbian-like networks and aminergic connections. We demonstrate here a major departure from this evolutionary trend in Brachyura, the most recent malacostracan lineage. In the shore crab Hemigrapsus nudus, instead of occupying the rostral surface of the lateral protocerebrum, mushroom body calyces are buried deep within it with their columns extending outwards to an expansive system of gyri on the brain’s surface. The organization amongst mushroom body neurons reaches extreme elaboration throughout its constituent neuropils. The calyces, columns, and especially the gyri show DC0 immunoreactivity, an indicator of extensive circuits involved in learning and memory.
more »
« less
- Award ID(s):
- 1754798
- PAR ID:
- 10491846
- Publisher / Repository:
- eLife
- Date Published:
- Journal Name:
- eLifePress
- ISSN:
- 2582-7944
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Descriptions of crustacean brains have focused mainly on three highly derived lineages of malacostracans: the reptantian infraorders represented by spiny lobsters, lobsters, and crayfish. Those descriptions advocate the view that dome- or cap-like neuropils, referred to as ‘hemiellipsoid bodies,’ are the ground pattern organization of centers that are comparable to insect mushroom bodies in processing olfactory information. Here we challenge the doctrine that hemiellipsoid bodies are a derived trait of crustaceans, whereas mushroom bodies are a derived trait of hexapods. We demonstrate that mushroom bodies typify lineages that arose before Reptantia and exist in Reptantia thereby indicating that the mushroom body, not the hemiellipsoid body, provides the ground pattern for both crustaceans and hexapods. We show that evolved variations of the mushroom body ground pattern are, in some lineages, defined by extreme diminution or loss and, in others, by the incorporation of mushroom body circuits into lobeless centers. Such transformations are ascribed to modifications of the columnar organization of mushroom body lobes that, as shown in Drosophila and other hexapods, contain networks essential for learning and memory.more » « less
-
IntroductionThe ‘social brain hypothesis’ proposes that brain development (particularly primates) is driven by social complexity, more than group size. Yet, small insects with minute brains are capable of the most complex social organization in animals - which warrants further attention. Research has focused on highly eusocial hymenopterans with extreme caste specialization and very large colony sizes that have passed social evolutionary points of no return. However, facultatively social insects that form small colonies (< 20 individuals) are likely to provide greater insight on brain selection at the origin-point of social group living. MethodsWe undertake the first neurobiological investigation of the facultatively social allodapine bees (Apidae: Xylocopinae: Allodapini), an exploratory study comparing single- and multi-female colonies ofExoneura angophorae. Using volume as a proxy for neural investment, we measured mushroom body calyces, optic lobes, antennal lobes and whole brains of queens, workers, and single-females to test three theories associating brain development with behavior: social brain hypothesis; distributed cognition hypothesis; sensory environment hypothesis. ResultsMushroom bodies were reduced in subordinate workers, but did not differ between queens and single-females. Workers had larger optic lobes than queens, but did not differ from single-females. There were no differences in antennal lobes or whole brain volume. DiscussionSocial caste, rather than multi-female versus single-female nesting, influenced mushroom body volume in this allodapine bee – counter to both social brain and distributed cognition theories and in alignment with halictine and ceratinine bees that also form small facultatively social colonies. Optic lobe enhancement is likely a response to dietary niche requirements for extra-nidal foraging behavior – which may be a highly plastic trait capable of rapid transition among allodapine and ceratinine bees that conforms with ecological intelligence hypotheses. These broad volumetric trends require further investigations on the functional neural circuitry involved in the aforementioned environmental contexts.more » « less
-
Sun, Qian “Karen” (Ed.)Abstract Social behavior has been predicted to select for increased neural investment (the social brain hypothesis) and also to select for decreased neural investment (the distributed cognition hypothesis). Here, we use two related bees, the social Augochlorella aurata (Smith) (Hymenoptera: Halictidae) and the related Augochlora pura (Say), which has lost social behavior, to test the contrasting predictions of these two hypotheses in these taxa. We measured the volumes of the mushroom body (MB) calyces, a brain area shown to be important for cognition in previous studies, as well as the optic lobes and antennal lobes. We compared females at the nest foundress stage when both species are solitary so that brain development would not be influenced by social interactions. We show that the loss of sociality was accompanied by a loss in relative neural investment in the MB calyces. This is consistent with the predictions of the social brain hypothesis. Ovary size did not correlate with MB calyx volume. This is the first study to demonstrate changes in mosaic brain evolution in response to the loss of sociality.more » « less
-
Brain centers possessing a suite of neuroanatomical characters that define mushroom bodies of dicondylic insects have been identified in mantis shrimps, which are basal malacostracan crustaceans. Recent studies of the caridean shrimp Lebbeus groenlandicus further demonstrate the existence of mushroom bodies in Malacostraca. Nevertheless, received opinion promulgates the hypothesis that domed centers called hemiellipsoid bodies typifying reptantian crustaceans, such as lobsters and crayfish, represent the malacostracan cerebral ground pattern. Here, we provide evidence from the marine hermit crab Pagurus hirsutiusculus that refutes this view. P. hirsutiusculus, which is a member of the infraorder Anomura, reveals a chimeric morphology that incorporates features of a domed hemiellipsoid body and a columnar mushroom body. These attributes indicate that a mushroom body morphology is the ancestral ground pattern, from which the domed hemiellipsoid body derives and that the “standard” reptantian hemiellipsoid bodies that typify Astacidea and Achelata are extreme examples of divergence from this ground pattern. This interpretation is underpinned by comparing the lateral protocerebrum of Pagurus with that of the crayfish Procambarus clarkii and Orconectes immunis, members of the reptantian infraorder Astacidea.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- The DOI is not currently available.
