Social regulation of a rudimentary organ generates complex worker-caste systems in ants

Rajakumar, Rajendhran; Koch, Sophie; Couture, Mélanie; Favé, Marie-Julie; Lillico-Ouachour, Angelica; Chen, Travis; Blasis, Giovanna De; Rajakumar, Arjuna; Ouellette, Dominic; Abouheif, Ehab

doi:10.1038/s41586-018-0613-1

Cited by 57 publications

(78 citation statements)

References 50 publications

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“…4A, solid line). This pattern is consistent with the general expectation that trait expression among castes from the same polyphenic series must be coupled to some degree, because they develop from a single genome and have limited pupal resources to repurpose during metamorphosis (15,16,26). Nevertheless, there was considerable variation among species in whether soldier heads are smaller, equal to, or larger than the head of the queen (Fig.…”

Section: Resultssupporting

confidence: 87%

“…present (12,20,24,25). Similarly, the phenotype of all castes within a polyphenic series must be coupled to some degree by developing from a single genome and having limited pupal resources to repurpose during metamorphosis, although the mechanisms and constraints governing caste development continue to be debated (15,16,26). Yet these insights, intimately connected with the general issues of reversibility, repeatability, and decoupling in trait evolution, may represent only the broad bounds of phenotypic change in social lineages.…”

Section: Significancementioning

confidence: 99%

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Trait evolution is reversible, repeatable, and decoupled in the soldier caste of turtle ants

Powell

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Kronauer

2020

Proc. Natl. Acad. Sci. U.S.A.

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The scope of adaptive phenotypic change within a lineage is shaped by how functional traits evolve. Castes are defining functional traits of adaptive phenotypic change in complex insect societies, and caste evolution is expected to be phylogenetically conserved and developmentally constrained at broad phylogenetic scales. Yet how castes evolve at the species level has remained largely unaddressed. Turtle ant soldiers (genusCephalotes), an iconic example of caste specialization, defend nest entrances by using their elaborately armored heads as living barricades. Across species, soldier morphotype determines entrance specialization and defensive strategy, while head size sets the specific size of defended entrances. Our species-level comparative analyses of morphotype and head size evolution reveal that these key ecomorphological traits are extensively reversible, repeatable, and decoupled within soldiers and between soldier and queen castes. Repeated evolutionary gains and losses of the four morphotypes were reconstructed consistently across multiple analyses. In addition, morphotype did not predict mean head size across the three most common morphotypes, and head size distributions overlapped broadly across all morphotypes. Concordantly, multiple model-fitting approaches suggested that soldier head size evolution is best explained by a process of divergent pulses of change. Finally, while soldier and queen head size were broadly coupled across species, the level of head size disparity between castes was decoupled from both queen head size and soldier morphotype. These findings demonstrate that caste evolution can be highly dynamic at the species level, reshaping our understanding of adaptive morphological change in complex social lineages.

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Section: Resultssupporting

confidence: 87%

Section: Significancementioning

confidence: 99%

Trait evolution is reversible, repeatable, and decoupled in the soldier caste of turtle ants

Powell

Price

Kronauer

2020

Proc. Natl. Acad. Sci. U.S.A.

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“…Soldiers are thought to have originated by modifying the developmental trajectory of queens [67], reprogramming worker larval growth rules [73], combining queen and worker developmental modules [68–70], or altering size-related caste determination mechanisms [72]. Recently, soldier development in Pheidole was found to be regulated by rudimentary wing discs [74]. Our macroscopic and synaptic study of caste- and subcaste-related brain structure in C .…”

Section: Discussionmentioning

confidence: 99%

Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians

et al. 2019

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Strongly polyphenic social insects provide excellent models to examine the neurobiological basis of division of labor. Turtle ants, Cephalotes varians, have distinct minor worker, soldier, and reproductive (gyne/queen) morphologies associated with their behavioral profiles: small-bodied task-generalist minors lack the phragmotic shield-shaped heads of soldiers, which are specialized to block and guard the nest entrance. Gynes found new colonies and during early stages of colony growth overlap behaviorally with soldiers. Here we describe patterns of brain structure and synaptic organization associated with division of labor in C. varians minor workers, soldiers, and gynes. We quantified brain volumes, determined scaling relationships among brain regions, and quantified the density and size of microglomeruli, synaptic complexes in the mushroom body calyxes important to higher-order processing abilities that may underpin behavioral performance. We found that brain volume was significantly larger in gynes; minor workers and soldiers had similar brain sizes. Consistent with their larger behavioral repertoire, minors had disproportionately larger mushroom bodies than soldiers and gynes. Soldiers and gynes had larger optic lobes, which may be important for flight and navigation in gynes, but serve different functions in soldiers. Microglomeruli were larger and less dense in minor workers; soldiers and gynes did not differ. Correspondence in brain structure despite differences in soldiers and gyne behavior may reflect developmental integration, suggesting that neurobiological metrics not only advance our understanding of brain evolution in social insects, but may also help resolve questions of the origin of novel castes.

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“…On the basis of these studies, M. pharaonis has been deemed to have three larval instars, and our data fully support this. In ants, the reported number of larval instars range from three to six (Solis et al 2010;Alvordo et al 2015;Rajakumar et al 2018). Little information is available in terms of duration of each instar in this species, as it is often difficult to obtain direct observation of larval moulting.…”

Section: Larval Developmentmentioning

confidence: 99%

From egg to adult: a developmental table of the antMonomorium pharaonis

Pontieri

Rajakumar

Rafiqi

et al. 2020

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Ants exhibit remarkable phenotypic diversity and, with over approximately 16,000 species across 6 continents, represent one of the most evolutionarily and ecologically successful groups of animals. All ants are eusocial with a reproductive division of labor between morphologically and/or behaviourally distinct castes within a single species. This has made ants an ideal system to study core questions of eco-evo-devo (ecological evolutionary developmental biology) by highlighting the role of developmental plasticity, epigenetics, ancestral developmental potentials, modularity, and major evolutionary transitions in the evolutionary process. Yet, despite their importance for eco-evo-devo, no complete ontological series for an ant has been published to date. We therefore present the first developmental table in ants, from egg to adult, for the Myrmicine ant Monomorium pharaonis. We identified and characterized 17 embryonic stages, 3 larval instars, and prepupal/pupal development. We found that the majority of landmarks identified during embryogenesis in the fruitfly Drosophila melanogaster are conserved in M. pharaonis. Furthermore, we can morphologically discriminate reproductive larvae (queen and male-destined larvae) from one another after the 1st larval instar. Finally, this ontological series of M. pharaonis will serve as a blueprint for the generation of future ant developmental tables, which is key to understanding how the remarkable diversity in ants evolved.

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Social regulation of a rudimentary organ generates complex worker-caste systems in ants

Cited by 57 publications

References 50 publications

Trait evolution is reversible, repeatable, and decoupled in the soldier caste of turtle ants

Trait evolution is reversible, repeatable, and decoupled in the soldier caste of turtle ants

Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians

From egg to adult: a developmental table of the antMonomorium pharaonis

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