Armed reproductives: Evolution of the frontal gland in imagoes of Termitidae
Introduction
Termites are ecologically dominant in a variety of tropical and subtropical habitats, where they are extremely abundant, representing a rich food source for a wide variety of predators (Deligne et al., 1981). The established colonies are well defended by passive adaptations such as a hidden way of life, or the nest and gallery architecture (Perna et al., 2008), and by active adaptations consisting in the presence of a rich set of morphological and behavioural defensive features in a specialized caste of defenders, the soldiers (Deligne et al., 1981; Šobotník et al., 2010a). Consequently, individuals residing inside the nest are well protected, but they are subjected to predation as soon as they leave the nest. Predation is known to be important, both on workers during foraging activities and on alate imagoes during dispersal flights and early phases of colony establishment (Dial and Vaughan, 1987; Lepage, 1991; Korb and Salewski, 2000).
During the combat, termites generally try to bite the opponent, and often combine the mandibular action with the release of a defensive secretion from specialized glands such as the labial glands (Moore, 1968; Plasman et al., 1999) or the labral glands (Quennedey, 1984; Šobotník et al., 2010b). Several taxa also developed their own innovative defensive strategies as exemplified by the dehiscent glands in Ruptitermes (Costa-Leonardo, 2004) or the dorsal apparatus in Neocapritermes taracua (Šobotník et al., 2012). However, the most prominent defensive organ of termites is undoubtedly the frontal gland, occurring in a clade comprising the families Rhinotermitidae, Stylotermitidae, Serritermitidae and Termitidae (Emerson, 1971).
The frontal gland is a structure without any equivalent among other animals (Noirot, 1969). In the soldier caste, it is an unpaired organ, epithelial gland with reservoir (according to classification Billen, 2011), opening at the top of the head through the fontanelle (Noirot, 1969; Prestwich and Collins, 1982; Quennedey, 1984; Šobotník et al., 2010d). It can either be restricted only to the head, as in many Termitidae (Noirot, 1969), or reach deep into the abdomen as in most Rhinotermitidae and Serritermitidae (Šobotník et al., 2004, 2010a). The frontal gland structure and secretion is well known in soldiers, but received almost no attention in other castes, even though it has been reported in presoldiers of some species (Prestwich, 1984a; Bordereau et al., 1997; Šobotník et al., 2004), in some workers (Šobotník et al., 2010c) and in all imagoes of Rhinotermitidae and Serritermitidae (Šobotník et al., 2010d). Contrary to the soldiers, the frontal gland is never epithelial with reservoir in workers, but occurs as an epithelial thickening only (Šobotník et al., 2010c). In imagoes, both forms are observed but up to now, only superficial descriptions have been published of Termitidae imagoes (Holmgren, 1909; Bugnion, 1913; Noirot, 1969).
The frontal gland of soldiers produces many classes of chemicals (hydrocarbons, alcohols, aldehydes, ketons, macrolactones, mono-, sesqui- and diterpenes, aromatic compounds, nitro-compounds, ceramids and others), which act as contact poisons, irritants, repellents, immobilizing agents, antihealants, or alarm pheromones (Howse, 1984; Prestwich, 1984b; Šobotník et al., 2010a). The composition of the frontal gland secretion of imagoes is known only in Prorhinotermes spp. (Rhinotermitidae), where it contains toxic and irritant chemical compounds, like the soldiers' secretion (Piskorski et al., 2007, 2009; Šobotník et al., 2010a).
To complete the story of the evolution of the frontal gland in termite imagoes, we investigated the anatomy of this gland in a representative set of Termitidae species. Termitidae is the most abundant family of termites, with the largest ecological and behavioural diversity, and contains over 85% of genera and 70% of species (Engel et al., 2009). In the present work, we studied the frontal gland in imagoes of 34 species, representing seven of the eight currently recognized Termitidae subfamilies (Sphaerotermitinae, Macrotermitinae, Foraminitermitinae, Apicotermitinae, Termitinae, Syntermitinae, and Nasutitermitinae sensu Engel et al., 2009).
Section snippets
Materials and methods
Specimens used for this study are listed in Table 1. They were either preserved in 80% alcohol or fixed for electron microscopy (for details, see Šobotník et al., 2010d). Semithin sections (0.5 or 1 μm thick) were cut with an Ultracut Reichert-Jung and stained with Azure II or toluidin blue solutions. Sections were studied with a Carl Zeiss Amplival microscope combined with a Canon EOS 500 D digital camera. All figures represent sagittal or parasagittal sections of heads of imagoes, with mouth
Common features of imaginal frontal glands
The frontal gland is always located posteriorly to the brain, behind the posterior attachment of the fronto-labral muscle. Two basic types of frontal gland were observed, either epithelial with or without the reservoir (the gland being present only as an epidermal thickening of lenticular or conical shape); glands of the latter type are generally smaller (Table 2). Because the shape of both types of frontal gland differs, we used two different equations to estimate the relative size of the
Discussion
The frontal gland is a defensive organ of prime importance in soldiers of advanced termites, occurring also in presoldiers, imagoes and workers (Quennedey, 1984; Šobotník et al., 2010a,c,d). While its structure and function is well-understood in soldiers, only scarce data on other castes have been gathered. The original form of the frontal gland was epithelial with reservoir, as evidenced by the reconstruction of its ancestral state in the common ancestor of all studied species. The frontal
Acknowledgements
We are grateful to Christian Bordereau and Kumar Krishna for providing part of material for this study. We are grateful to Mirek Hyliš for the help with TEM. This research was funded by the Czech Science Foundation (project No. P506/10/1570), by the Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, Prague (project RVO: 61388963). JŠ thanks to project 20124364 of Internal Grant Agency of Faculty of Forestry and Wood Sciences (Specific research of the
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