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Macroevolutionary integration of phenotypes within and across ant worker castes.

ABSTRACT: Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies, the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genus Pheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus, Pheidole workers are evolving as a mixture of intracaste and intercaste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.

SUBMITTER: Friedman NR

PROVIDER: S-EPMC7487254 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Macroevolutionary integration of phenotypes within and across ant worker castes.

Friedman Nicholas R NR Lecroq Bennet Beatrice B Fischer Georg G Sarnat Eli M EM Huang Jen-Pan JP Knowles L Lacey Knowles LLK Economo Evan P EP

Ecology and evolution 20200818 17

Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies, the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of h ...[more]

PMID: 32953067

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Project description:Certain species of parasitic flies belonging to the Phoridae are known to attack Atta spp. workers foraging along trails, near nest openings used by the ants to supply the colony with plant material, and in the areas where the ants are actively cutting plant material. However, there have been no previous studies of phorid parasitism of non-foraging worker ants, for example excavators and soldiers. Excavators can be found on the surface around specialized nest openings, carrying and dumping soil on characteristic mounds. Soldiers can be found on the trails protecting foragers or guarding the different types of nest openings. The current study was performed to investigate the differential parasitism rates of Atta laevigata (Smith, 1858) worker castes by four species of phorids. Ants of all castes on trails and at nest entrances were collect from 18 mature colonies in the field. A total of 21,254 ants were collected from trails and 14,649 collected from the mounds of loose soil near nest openings. The captured workers were maintained under controlled laboratory conditions to evaluate the rate of parasitism. Of the ants collected from trails, 1,112 (5.23%) were found to have been parasitized, of which 1,102 were foragers and only 10 were soldiers. Of the ants collected from the soil mounds near the nest openings, only 27 (0.18%) were found to have been parasitized, of those 25 were excavators and 2 were soldiers. When evaluating parasitism of ants on the trails, 46.2% were attacked by Apocephalus attophilus Borgmeier, 1928, 22.6% by Myrmosicarius grandicornis Borgmeier, 1928, 16.6% by Eibesfeldtphora erthali (Brown, 2001) and 14.6% by Apocephalus vicosae Disney, 2000. Only two species of phorid, M. grandicornis and E. erthali, were observed parasitizing excavators, whilst only E. erthali parasitized soldiers. This is the first time that Atta spp. excavators and soldiers have been shown to be parasitized by phorids. The low rates of parasitism and specificity of certain phorid species for excavators and soldiers is discussed in relation to the behavioral interactions of hosts and their parasitoids, as well as the relationship between host and parasitoid size.

Project description:BackgroundCamponotus floridanus ant colonies are comprised of a single reproductive queen and thousands of sterile female offspring that consist of two morphologically distinct castes: smaller minors and larger majors. Minors perform most of the tasks within the colony, including brood care and food collection, whereas majors have fewer clear roles and have been hypothesized to act as a specialized solider caste associated with colony defense. The allocation of workers to these different tasks depends, in part, on the detection and processing of local information including pheromones and other chemical blends such as cuticular hydrocarbons. However, the role peripheral olfactory sensitivity plays in establishing and maintaining morphologically distinct worker castes and their associated behaviors remains largely unexplored.ResultsWe examined the electrophysiological responses to general odorants, cuticular extracts, and a trail pheromone in adult minor and major C. floridanus workers, revealing that the repertoire of social behaviors is positively correlated with olfactory sensitivity. Minors in particular display primarily excitatory responses to olfactory stimuli, whereas major workers primarily manifest suppressed, sub-solvent responses. The notable exception to this paradigm is that both minors and majors display robust, dose-dependent excitatory responses to conspecific, non-nestmate cuticular extracts. Moreover, while both minors and majors actively aggress non-nestmate foes, the larger and physiologically distinct majors display significantly enhanced capabilities to rapidly subdue and kill their adversaries.ConclusionsOur studies reveal the behavioral repertoire of minors and majors aligns with profound shifts in peripheral olfactory sensitivity and odor coding. The data reported here support the hypothesis that minors are multipotential workers with broad excitatory sensitivity, and majors are dedicated soldiers with a highly specialized olfactory system for distinguishing non-nestmate foes. Overall, we conclude that C. floridanus majors do indeed represent a physiologically and behaviorally specialized soldier caste in which caste-specific olfactory sensitivity plays an important role in task allocation and the regulation of social behavior in ant colonies.

Dataset Information

Macroevolutionary integration of phenotypes within and across ant worker castes.

Publications

Macroevolutionary integration of phenotypes within and across ant worker castes.

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