Caste-Specific Morphological Modularity in the Ant Tribe Camponotini (Hymenoptera, Formicidae) A
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Laciny et al. BMC Zoology (2019) 4:9 https://doi.org/10.1186/s40850-019-0048-7 BMC Zoology RESEARCH ARTICLE Open Access Caste-specific morphological modularity in the ant tribe Camponotini (Hymenoptera, Formicidae) A. Laciny1,2* , H. L. Nemeschkal1, H. Zettel2, B. Metscher1 and I. S. Druzhinina3,4 Abstract Background: The morphological structures of organisms form tightly integrated but mutually independent character complexes (modules) linked through common development and function. Even though their abundance, diversity, and complex caste systems make camponotine ants ideal subjects to research developmental modularity and phenotypic integration, no studies investigating these phenomena have been conducted in this taxonomic group. This study attempts to identify and visualize integrated character complexes in 14 taxa from the genera Camponotus and Colobopsis using statistical analyses of morphometry. Results: The identified modules differ between castes: Minor workers have small heads and long extremities, while major workers have enlarged heads modified for defence, and short, thick appendages; extremities (legs and antennae) are strongly correlated in both worker castes. Gynes show weaker integration of extremities, but a strong correlation of mesosoma and eyes, and highly variable median ocellus size. Gynes infested by mermithid nematodes exhibit reduction of gyne-specific characters and altered patterns of phenotypic integration. Conclusion: The integrated character complexes described herein can largely be interpreted as functional, caste- specific modules related to behavioural ecology and task allocation within ant colonies. This modular nature of the body plan is hypothesized to facilitate the evolution of novel phenotypes and thus contributes to the tremendous evolutionary success of ants. The study of these modules can help to further elucidate the evolution and ontogeny of castes in camponotine ants, as well as the effects of parasite infestation on the phenotype. Keywords: Cluster analysis, Division of labour, Modules, Morphometry, PCA, Social insects, Phenotypic integration Background morphological, genetic, or otherwise – exhibit strong Phenotypic integration and modularity interconnection and correlation, but are relatively inde- The concept of phenotypic integration was first popular- pendent of other such groups, thereby dividing organisms ized in 1958 by Olson & Miller [1]. It states that, when into distinct, heterogeneous parts or “modules”. The con- viewing an organism as a whole, certain morphological cept of modularity has gained great interest in the fields of structures covary more strongly than others, forming evolutionary, developmental, and systems biology within spatially and temporally interdependent modules due to the last decade [2–4]; for reviews see [5–8]. commonalities in development and function. It thereby While most research on the phenomenon has been becomes evident that the concept of phenotypic integra- performed on vertebrates [1, 3, 9–11] and flowering tion is closely linked to the topic of modularity: In plants [12, 13], insects are rather poorly studied in this most known organisms, certain groups of elements – regard [14]. Depending on the investigated traits and applied methodology, previous authors have reported * Correspondence: [email protected] either intermediate [15, 16] or very high [14, 17] levels 1Department of Theoretical Biology, University of Vienna, Althanstraße 14, of phenotypic integration in holometabolous insects. 1090 Vienna, Austria To date, there have been very few studies directly in- 2Natural History Museum Vienna, 2nd Zoological Department, Burgring 7, 1010 Vienna, Austria vestigating how patterns of integration and modularity Full list of author information is available at the end of the article differ between castes and species of the family © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Laciny et al. BMC Zoology (2019) 4:9 Page 2 of 20 Formicidae and none in the diverse tribe Camponotini. Camponotus in its current state, his results indicated a Most studies investigating integration and modularity gradual transition from monophasic allometry to in ants are either conceptual in nature [18, 19]orfocus complete dimorphism of the worker caste, which has on single phenotypes or species [20–22]. Some note- arisen independently multiple times. He especially men- worthy exceptions are publications describing caste- tioned the pronounced dimorphism within the current specific patterns of modularity in Pheidole [17]or genus Colobopsis, where the specialized major workers highlighting trade-offs and correlations between defen- bear plug-shaped heads used to close the small sive structures in ants [23]. Comparing such phenom- entrance-holes in wooden nests. This phenomenon of ena across ant castes and taxa is especially intriguing: animals using parts of their bodies to obstruct their Firstly, the workers of a colony are closely related and nests is termed “phragmosis”. Several cases of independ- the diversity of castes has been attributed to high de- ent evolution of diverse phragmotic structures have also grees of phenotypic plasticity and modularity [18, 19, been described in at least five other genera and subgen- 24, 25]. Secondly, phenotypically integrated modules era of ants [33]. frequently correspond to structures associated with Most traditional theories assume the origin of the major particular functions and behaviours, e.g. locomotion, worker or soldier caste from minor workers [37, 38]. Other foraging, or defence [10, 11, 17, 23] and may thus be authors, however, have strongly disputed this, regarding connected to phenomena of functional specialization majors as a caste derived from queens. This assumption is and division of labour commonly observed in ants exhi- based on many morphological similarities and observations biting morphologically distinct castes. By analysing of larval development [39, 40]. More recent publications, caste- and species-specific patterns of integration and however, propose the evolution of specialized castes as mo- modularity, we can therefore gain a better understand- saics of pre-existing or ancestral developmental patterns ing of the functional and ecological roles of morpho- [18, 24, 41]. Others consider the influences of genetic and logical structures and character-sets. epigenetic mechanisms [42], disruptive selection [43], or hormonal regulation [44] on caste evolution, leaving the Caste-specific morphological specializations in issue open to further investigation. Camponotini In addition to the genus-specific phragmotic major The ant tribe Camponotini currently includes 1896 spe- workers, minor workers of the Southeast Asian Colobop- cies in eight genera [26–28]. Females of the campono- sis cylindrica (COCY) group (Figs. 1a, b, d; 2a, c, e) have tine species are particularly known for their diversity of evolved a peculiar specialization as well: In territorial morphologies within the worker caste [29–32]. The combat with other arthropods, they can rupture their most prominent cases of worker caste dimorphism are enlarged mandibular gland reservoirs and their gastral found in the genera Camponotus, Colobopsis and Dino- integument, thereby covering their enemy in a sticky, myrmex: most commonly, the smaller minor workers toxic defensive secretion and sacrificing their own lives (Fig. 1) engage in foraging, brood care and nest- in the process [31, 32, 45–49]. The roughly 15 species maintenance, while the major workers (often termed included in the group have been preliminarily divided “soldiers”) have large heads and mandibles specialized into four subgroups (complexes) based on molecular for defence [28, 30, 33](Fig.2a, b, d, f). and morphological data (Zettel et al., in prep.). Members Alate sexuals (gynes and males) in the Camponotini of the Colobopsis saundersi (Figs. 1a; 2a, c, e), C. leo- are typically characterized by large eyes and ocelli, and nardi (Fig. 1b) and C. cylindrica (s. str.) (Fig. 1d) com- an enlarged mesosoma to accommodate the flight mus- plexes are treated in the present study. cles [34, 35]. In contrast to the larger gynes (Fig. 2c), One especially intriguing aspect of the hitherto investi- males usually have a small body and head, as well as gated COCY colonies is the frequent presence of so- long and fragile extremities [33]. Their short lifespans called “interlopers” [31, 48, 50] – presumably mimetic [36] and mating flights make them much harder to sam- and parabiotic ants belonging to Camponotus (Myrmam- ple than their conspecific females, leading to their scar- blys) (Figs. 1e, 2f), whose minor workers are often found city in museum collections and low number of publications inside COCY nests [50]. The inclusion of the example describing male phenotypes. As males of the Camponotini species Camponotus inquilinus in this study aims to fur- are still insufficiently studied and taxonomic relationships ther assess their morphology