Reflections on structure and function of pheromone glands in storage insect species

Several polyphagous coleopteran and lepidopterous species, presently known as storage insects, have presumably evolved from free-living ancestral species, being capable of growth and reproduction on stored, desiccated and often nutritionally deficient foodstuffs. These potentially harmful insect species have probably adapted themselves to the newly acquired storage biotope by means of a well-developed sensory equipment serving food acquisition, aggregation and mate finding.Information by molecules may be communicated among the individuals of an insect species by means of relatively volatile pheromones (Greek, pher=convey) being emitted by exocrine glands and mainly carried by moving air to the sensilla of responsive individuals, or among the internal organs of an insect by means of relativelynonvolatile hormones (Greek, horma=impel), secreted fromendocrine glands and transported by the haemolymph to the receptors of target organs. It was postulated that pheromones were among the first chemical messengers utilized during evolution of animal behaviour, and that the pheromones of primitive protozoans could have been precursors of the hormones of metazoans. Hormones of the neurosecretory cells and corpora allata were found to induce sex pheromone biosynthesis in femaleTenebrio molitor, while dietary intake of a juvenile hormone analogue was shown to significantly enhance the production of aggregation pheromones in the males of certain silvanid and cucujid species.Aggregation pheromones are usually produced by the longlived and feeding males of several coleopteran species (Table 2) which deposit those chemical messengers to the substrate, where they induce the formation of bisexual assemblies supporting feeding, mating and reproduction. Sex pheromones are mostly produced by the short-lived and non-feeding females of several coleopteran and lepidopterous species (Table 2); females of those species usually release their sex pheromones to the air space during calling, and thus attract conspecific males for mating (Fig. 5 a–c).In some dermestid species, pheromone emission differs from the above scheme. Females of the short-lived and non-feedingTrogoderma granarium andT. inclusum release a phromone acting as a sex attractant for conspecific males and—in synergistic combination with tactile stimuli—as an assembling scent for conspecific females (Figs. 1 a, b, 2 and Table 1), females of the short-lived and feedingAntbrenus verbasci, Attagenus megatoma andAtt. elongatulus produce a sex pheromone for conspecific males, while females of the long-lived and feedingAn. scrophulariae emit a sex pheromone which lures conspecific males.Males of the long-lived and non-feeding bruchid speciesAcanthoscelides obtectus release a sex pheromone which attracts conspecific females. Androconial pheromones are discharged during courtship from the alar scales and abdominal tufts found in males of several microlepidopteran species (Phycitidae) includingAnagasta kuebniella, Cadra cautella, Ephestia elutella andPlodia interpunctella (Fig. 6 b–c); those aphrodisiac pheromones are known to enhance the specific responsiveness of the females to their mates. Electrophysiological recordings revealed that aggregation pheromones elicit considerable receptor potentials in the antennal olfactory sensilla of both sexes, whereas sex pheromones induce high receptor potentials in the antennal olfactory sensilla of one sex only. It was assumed that aggregation pheromones may be the evolutionary precursors of sex pheromones.Pheromone-producingexocrine glands are essentially groups of modified epidermals cells which are found in different body regions of male and/or female storage insect species. A simple pheromone gland, consisting of a single layer of adjacent secretory cells beneath the endocuticle of the 5th visible abdominal sternite, occurs in femaleTrogoderma granarium (Fig. 3 a). A more complex design, comprising an intra-abdominal semiglobular pheromone gland with numerous secretory cells being connected to tubuli which lead to an invaginated cuticular cribellum, is available in maleDermestes maculatus (Figs. 3 c, d and 4 c). The cribellum, provided with a caudally curved brush of fluted brisles, occurs in the centre of the 4th visible abdominal sternite (Figs. 4 a, b and 7 b). An apodemous exocrine gland is found in the lumen of the second abdominal segment of femaleLasioderma serricorne (Fig. 3 b). This lobate gland comprises many secretory cells, being connected by numerous tubuli to a sheath-like conical duct enveloping a V-shaped skeletal apodeme, which terminates in the abdominal tip. In maleTribolium castaneum, the secretory cells of both pheromone glands are connected by tubuli to two cribella, being densely covered by fluted bristles, and found in the femora of both forelegs (Fig. 7 a). Females of the phycitid speciesAnagasta kuebniella, Cadra cautella, Ephestia elutella andPlodia interpunctella are equipped with an intersegmental pheromone gland, situated between the 8th and 9th abdominal segment near the genital opening. The exocrine gland of the four moth species consists of a single layer of columnar secretory cells, lined by a spongy cuticle which seems to be permeable to the sex pheromone (Fig. 6 a). The latter is disseminated by calling females (Fig. 5 a, b) while their exocrine glands are widely exposed. Males of the above phycitid species are furnished with alar and abdominal androconia which become exposed during courtship and discharge aphrodisiac pheromones. The base of each of the androconial bristles and scales is immersed to an underlying unicellular, pheromone-producing gland (Fig. 6 d, e). The aphrodisiac pheromones, being secreted by the above glandular cells, are passing the lumen and walls of the bristles and scales, and evaporate from the surface of the latter. For example, malePlodia interpunctella possess 2 pairs of scent tufts (a small and a large one) on both sides of the 8th abdominal tergiet as well as 2 pairs of scent tufts (a small and a large one) near the base of the costal margin of the forewings (Fig. 6 b, c). Females of several phycitid species respond to the aphrodisiac pheromone of conspecific males by a pronounced readiness to mate.In the course of time, about 3 dozens of insect species (3/4 coleopteran and 1/4 lepidopterous species) have undergone sympatric speciation by sharing desiccated food in stores as a common habitat. Fertile matings between such heterogeneous species are often prevented by morphological and anatomical incompatibilities as well as physiological and behavioural barriers. Most of the species living in the storage habitat are reproductively isolated due to the molecular structure and blend composition of their pheromones (Table 2). Interestingly, some species (listed below) deviate from the majority by sharing the structure of their main pheromone components (mentioned in parenthesis), and are thus poorly separated: the curculionidsSitophilus oryzae andS. zeamais ((4S,5R)-5-hydroxy-4-methyl-3-heptanone), the tenebrionidsTribolium castaneum andT. confusum ((4R,8R)-dimethyldecanal) as well as the dermestidsTrogoderma inclusum andT. variabile ((R,Z)-14-methyl-8-hexadecenal). Theinsufficient reproductive isolation of the above species is compensated, i.a., by additional availability of a sex pheromone in femaleTribolium confusum, by different calling periods and emission rates of (R,Z)-14-methyl-8-hexadecenal in females of the forementionedTrogodema species.Trogoderma glabrum andT. granarium areincompletely isolated by sharing (R,E)-14-methyl-8-hexadecenal as a pheromone component; they are indeed capable of cross-mating, but produce sterile hybrids. Moreover, maleOryzaepbilus mercator andO. surinamensis incorporate (Z,Z)-3,6-dodecadien-11R-olide as a common chiral component to their aggregation pheromones. The females of 5 phycitid species share (Z,E)-9,12-tetradecadien-1-yl acetate as their main pheromone component, while they are reproductively separated by additional emission of (Z)-9-tetradecen-1-yl acetate and (Z,E)-9,12-tetradecadien-1-ol as secondary pheromone components, by the production of different androconial pheromones in conspecific males as well as different circadian calling activities.In the course of their research engagement on pheromones of storage insect and mite species (during the past 2.5 decades), the authors enjoyed fruitful collaboration with several renowned investigators working in Athens, Berlin, Hamburg, New York, Pantnagar, Tiantsin, Tokyo, Wisconsin, Yokohama and Zürich (chapter 6).Motto ...In addition to the amazing range of physiological activities of which it is capable during the process of moulting and cuticle formation, the epidermal cell is potentially an embryonic cell, with latent powers of differentiating in several different directions. The ordinary epidermal cell may divide to give rise to a pair of oenocytes. It may divide into four and produce a dermal gland cell with associated cells that form the glandular duct. Or the four daughter cells may differentiate into the bristle-forming and socket-forming cells which give rise to the sensillum and into the sense cell with its neurilemma cell both of which grow inwards to become a part of the central nervous system ...V B. Wigglesworth, 1959With 2 tables and 7 figuresDedicated to the memory of Prof. Dr. Sir Vincent BrianWigglesworth who died on February 12th, 1994.