Male pheromones in relation to the origin of the pheromone system in Lepidoptera*
Феромоны самцов в связи с происхождением феромонной системы чешуекрылых
All-Russian Institute for Plant Protection, Russian Academy of Agricultural Sciences, Podbelskogo 3, St.-Petersburg-Pushkin 189620 Russia.
Всероссийский научно-исследовательский институт защиты растений РАСХН, шоссе Подбельского, 3, С.-Петербург, Пушкин 189620 Россия.
KEY WORDS: Lepidoptera, chemical ecology, male sex pheromones, evolution.
КЛЮЧЕВЫЕ СЛОВА: Lepidoptera, химическая экология, половые феромоны самцов, эволюция.
ABSTRACT: A review of the chemical structure and functional role of Lepidoptera male pheromones is presented. Origin of the system of chemical communication in moths and butterflies is discussed. Male pheromones are relatively poorly understood, as compared to female pheromones in Lepidoptera and other insects. However, they are highly original in chemical composition and have a great variety of functions, which permits the knowledge of moth pheromone system to be used in the analysis of origin and evolution of the pheromone system of insects, and in the investigation of the significance of this system in chemical communication of living beings. From the data available it can be concluded that the pheromone composition in Lepidoptera and, possibly, other phytophagous insects is determined by the chemical composition of host plants. The number of biochemical changes in the biosynthesis chain may vary with species. Since pheromone biosynthesis tends to simplify the chemical structure of a precursor, we may have the rule: the more simplified the chemical structure of a pheromone, the longer the chain of its biosynthesis from a plant precursor and the wider the distribution and richer the behaviour functions of the pheromone components. And the second rule is: the rarer a plant precursor, the shorter the chain of pheromone biosynthesis and the more specialised the pheromone function. Evolution of the pheromone system of different insect groups has stopped at different stages. In the process of evolution it has reached independence of trophics in many insects. In view of fundamental studies, the prospects for the use of male pheromones in plant protection are also discussed.
РЕЗЮМЕ: В статье представлен обзор химической структуры и функциональной роли феромонов самцов у чешуекрылых насекомых. Обсуждается вопрос о происхождении системы феромонной коммуникации у бабочек. Феромоны самцов относительно слабо изучены по сравнению с феромонами самок чешуекрылых и других насекомых. Однако они имеют высокую степень оригинальности химического состава и большое функциональное разнообразие, что позволяет использовать знания о феромонах бабочек в анализе происхождения и эволюции феромонной системы насекомых и исследовании значения этой системы в химической коммуникации живых существ. Известные данные говорят о том, что компонентный состав феромонов чешуекрылых и, вероятно, других насекомых-фитофагов обусловлен химическим составом кормовых растений. В разных таксонах бабочек число биохимических преобразований в цепи биосинтеза может быть различным. Учитывая, что биосинтез феромонов часто идет по пути упрощения химической структуры предшественника, здесь, вероятно, действует правило: чем проще химическая структура феромона, тем длиннее цепь биосинтеза феромона из растительного предшественника, шире распространение и богаче поведенческие функции феромонных компонентов. Второе правило может быть сформулировано так: чем реже встречается растительный предшественник, тем короче цепь биосинтеза феромона, а его функция более специализирована. Феромонная система различных групп насекомых находится на разных стадиях эволюции. В процессе эволюции она достигла независимости от трофики у многих насекомых. С учетом фундаментальных исследований в статье также обсуждаются перспективы использования феромонов самцов в защите растений от вредителей.
Chemical communication is a widely spread phenomenon among animals and plants. Cueing substances have been identified both for unicellate algae and higher primates [Shorey, 1976]. However, it is the insects that have developed the most complete system of inter- and intraspecific communication by olfactory cues. By 1986, the list of sex attractants for Lepidoptera alone covered about 1000 species [Arn et al., 1986, and supplements]. Now it has reached at least 1500 species, whereas the total number of insect species for which pheromones are known is probably coming to 3000. Most sex attractants have become known as a result of extensive or directed field screening.
It must be realised, however, that of a huge iceberg of insect pheromone system only the top has been studied so far. Thus, for instance, the complete composition of pheromone glands of females has been investigated only for several dozens of species. Each pheromone can have 20 or more components of various functional roles. For the majority of moths, only 1 or 2 component words of their chemical language are known. Male pheromone components have been identified only for 45 species of Lepidoptera [Birch & Hefetz, 1987], though there is little doubt that they are present in males of most species of moths. The same applies to female pheromones.
More thorough studies have been made of sex attractants, and here it should be noted that females of about 700 species of Tortricidae and Noctuidae attract males using a set of only 170 chemicals [Grichanov, 1991]. There is a kind of periodic system in distribution of various chemicals among particular moth groups, and recently this encouraged some scientists to make, using electronic computers, cladistic schemes of taxonomic relations in Lepidoptera, on the basis of chemical structure of their sex pheromones [DorИ et al., 1986; Renou et al., 1988; Grichanov, 1993]. Although our knowledge of male moth pheromones is rather limited, the data available still permit some insight into the evolution of chemical communication in insects in general.
PHEROMONES OF LEPIDOPTERA MALES
Males of many species of nocturnal Lepidoptera have special organs associated with scent glands, secretions of which are sometimes perceptible even for man. These may be rather large and protruding bifurcate formations (coremata) on genital segments in Arctiidae, well developed hair-pencils at the base of abdomen in noctuid moths of subfamilies Hadeninae [e.g., Mamestra brassicae (L.)], Amphipyrinae (e.g., Apamea spp.), Cuculliinae, Noctuinae, and in the pyralid moth Ephestia elutella Hbn. (Pyralidae, Phycitinae), wing glands and brushes in many pyralids (Galleriinae), as well as in Geometridae and some leaf rollers, and finally, genital hair-pencils in a large number of noctuids, leaf rollers and other moths. Specialised scent organs are located on tarsi in noctuids, and on abdomen in Sphingidae and diurnal moths. Males of many nocturnal Lepidoptera have a whole system of scent organs. Thus, for instance, Paralispa gularis (Zeller) has wing and abdomen glands, while Trichoplusia ni (Hbn.) has brushes at the base of abdomen and on genitalia, etc.
The identified compounds include aldehydes (benzaldehyde, phenyl acetaldehyde, undecanal, octadecanal, carboxyaldehydes and others), acids (butanoic, benzoic, acetic and others), alcohols (phenyl ethanol, benzol, methyl heptenol, trans-phytol), lactones (decalactone, methyl-dimethyl-allyl-y-lactone), terpenes (pinocarvone, methyl heptenone, vanilline), esters (phenyl ethanol acetate, diethyle malonate, methyl jasmonate, ethyl cinnamate) and some others.
The data obtained suggest that for a number of species and families male pheromone composition is rather specific. In some cases, however, species specificity has not been supported. The main components of pheromones include aromatic alcohols, acids and aldehydes for noctuids, pyrrolizidine ketones for Danainae and pyrrolizidine lactones for Ithomiinae. Then comes heneicosatriene for a single known representative of Agaristidae, farnesal for Bapta temerata (Den. et Schiff.), and mellein and esterifying acids (jasmonic and cinnamic) for Grapholitha molesta (Busck.). Highly varied is pheromone composition in pyralid males, including cyclic alcohols and aldehydes, unsaturated aldehydes, lactones, vanilline and nonadienolide.
Often males of non-related species can have pheromone components of similar or even identical structure, e.g. pyrrolizidine alkaloids [Boppre, 1990]. It has been shown, that males of the genera Pyrrharctia and Creatonotos can also attract individuals of other insect species [Krasnoff & Dussourd, 1989; Boppre, 1990], and this may be explained by the fact that hydroxydanaidal acts not only as insect pheromone but as plant attractant as well.
In general, the number of active components of male pheromones is much lower than the number of moth species studied. That means that males, as well as females, rather efficiently consume energy resources for biosynthesis of new compounds.
In literature, the question has been repeatedly discussed concerning the mechanisms of reproductive isolation in great many of species having similar pheromone communication system [see Grichanov et al., 1994, 1995]. The answer may be as follows: the populations of species with identical set of attractive components are usually separated in space (geographically or ecologically) or in time, so that individuals do not come into contact with each other (geographical, seasonal and biotopic isolation [Mayr, 1974]). In those few cases when adults of such species fly concurrently the reproductive isolation is mediated by pheromone components (synergists and inhibitors), component ratio and emission rate. If even these mechanisms fail to work, ethological and physiological barriers arise (Mayr's ethological, mechanical and postcopulation isolation).
However, the Roelofs' hypothesis of taxonomic specificity of pheromone chemical composition [Roelofs & Brown, 1982] has not been supported for all insects. For bark beetles [Francke et al., 1989], chrysomelids [Metcalf & Lampman, 1989] and arctiids [Krasnoff & Dussourd, 1989], a close relation has been found between the pheromone composition of scent glands and chemical composition of host plants, which is compatible with the trophic hypothesis offered by Riddiford and Hendry [Riddiford, 1967; Hendry et al., 1975] and further developed by Skirkyavichus .
Usually, male pheromones significantly differ in chemical
structure from these of conspecific females. However, heneicosatriene,
a component that attracts males and at the same time disrupts courtship
communication in Phalaenoides glicinae Levin, has been found both
in males and females [Heath et al., 1988]. Also, cis-11-tetradecenal, one
of the pheromone components of Heliothis virescens (F.) females,
has been found in males too [Jacobson et al., 1984]. Subsequently, a more
precise identification indicated the presence of only acids, alcohols and
acetates, the latter including those corresponding in structure to all
six aldehydes of the female sex attractant [Teal & Tumlinson, 1989].
Also, biosynthesis of alcohols from acetates has been experimentally supported,
this being in contrast with the mechanism of production of attractive components
in females of some other species. A precursor of the female pheromone has
been found in males of Ceramica picta (Harris) [Butler et al., 1972].
Pheromones similar in structure to pyrrolizidine alkaloids of plants are
released only by males but often perceived both by males and females [Birch
& Hefetz, 1987; Boppre, 1990]. Females of these species (at least in
the Arctiidae) also use for chemical communication alkenol derivatives
which are common for moths [Arn et al., 1986].
LEPIDOPTERA MALE PHEROMONES IN RELATION TO INSECT BEHAVIOUR
The functional role of lepidopteran male pheromones has been so far poorly understood. However, there is hardly any doubt that they are of prime importance in courtship behaviour of moths.
Based on the data collected for some moth species, it may be suggested that pheromones from morphologically isolated glandular tissues have different functions. The problem is that in relation to insect behaviour pheromones were studied as a whole while they represent multicomponent substances varying with species. The male pheromone may contain about 50 compounds [Schulz, 1987]. For the present, one can only guess about the functions of particular identified components. Some of them may be precursors (propheromones) or intermediate products in the biosynthesis of active components, while others are, probably, neutral, inhibitory, attractive or synergistic compounds.
The role of male chemical signals in communication of sexes may vary with species. For practical reasons, the cases of long-range female-by-male attraction are of particular interest. They are known only for arctiids of the genera Estigmene and Creatonotos, pyralid Achroia grisella (F.), agaristid Phalaenoides glicinae and ithomiines (Nymphalidae). Recently, it has been found, that hydroxidanaidal, the main component of the arctiid male pheromone, just like plant alkaloids, attracts both sexes in Cisseps fulvicollis Hbn., Ctenucha virginica Char. and Halisidota tessellaris J.E. Smith [Krasnoff & Dussourd, 1989; Krasnoff & Roelofs, 1989]. In these studies it has been experimentally shown that larval feeding on diets deprived of pyrrolizidine alkaloids resulted in a reduced production of pheromone by male glands (by a factor of 100 or 1000). Since arctiid male pheromones are derivatives from plant attractants, the male pheromone function should be considered here as aggregational, rather than reproductive.
For Trichoplusia ni, Paralispa gularis, Galleria melonella and Grapholitha molesta, the short range (1 to 2 m) female by male attraction has been established. For the pyralids and G. molesta, the pheromone composition has also been identified [Birch & Hefetz, 1987].
For most noctuid and other moths there is no evidence for males being attractive to females. However, many antennographic and behavioural tests showed that females (and sometimes males) do respond to male aphrodisiacs. It has been often reported that these substances inhibit sexual activity of conspecific males or deter them and at the same time stimulate nuptial behaviour in females [Alpin & Birch, 1968; Birch, 1971; Hirai et al., 1978; Phelan & Baker, 1986; Teal & Tumlinson, 1989]. In contrast, other authors suggest that the function of the male pheromone is to inhibit female rejection behaviour [Clearwater, 1972; Fitzpatrick & McNeil, 1988] or to suppress emission of sex pheromone by females [Hendricks & Shaver, 1975], or to attract conspecific males and to disrupt their courtship behaviour [Heath et al., 1988].
Based on the finding that Utetheisa ornatrix (L.) males that have a decreased hydroxidanaidal content of their pheromone glands fail in courtship behaviour, Conner and Eisner suggested that females can choose males of a high ability to use pyrrolizidine alkaloids, and that this ethological character can be inherited [Eisner, 1980; Conner et al., 1981]. Bearing in mind that females receive considerable amounts of pyrrolizidine alkaloids from males in spermatophores [Brown, 1984, 1987], so that these compounds incorporate into eggs thus providing them some defence from predators [Dussourd et al., 1988], the following hypothesis was offered: Being the derivative from defence compounds transferred with such a "wedding present", the male pheromone helps the female to learn how much of necessary compounds it could receive during mating [Eisner & Meinwald, 1987, Dussourd et al., 1988]. There is supporting evidence for intersexual selection for this character in Utetheisa [Conner et al. in Birch & Hefetz, 1987]. In Creatonotos gangis (L.) and C. transiens (Walker) the choice of males may be also determined by the size of male coremata which is directly proportional to their pyrrolizidine alkaloid content.
ORIGIN OF THE PHEROMONE SYSTEM OF LEPIDOPTERA
The system of chemical communication in moths and butterflies is undoubtedly more complicated than described up-to-date. Sex pheromones of arctiid and nymphalid males are derivatives from pyrrolizidine alkaloids of their host plants. For other butterflies, so far there has been no good support for direct relation between host plants and pheromones. However, it has long been reported that many substances known as insect sex pheromones are present in plants as pheromone sources [Hendry et al., 1975]. Subsequently, both rejecting [Miller et al., 1976; Carde & Taschenberg, 1984; McNeil & Delisle, 1989] and supporting [Riddiford, 1967; Herrebout & van der Water, 1982; Raina, 1988] evidence has been obtained for this idea.
It has been clearly established that the known pheromones of moths are mostly synthesised de novo [Bjostad et al., 1987; McNeil & Delisle, 1989]. But the compounds most common in the Plant Kingdom, such as pentanol, E-3-hexenol, geraniol, eugenol, butanal, E-2-hexenal, salicilaldehyde, citral, benzaldehyde, benzyl acetate, butyl acetate and 2-hendecanone [Hansson et al., 1989], are very close to sex pheromone components and precursors [Bjostad et al., 1987] and include electrophysiological and ethological response in one or both sexes.
Aromatic compounds and low-molecular acids found in male
pheromones of noctuids and pyralids are also chemically related to plant substances of phenolic and acidic nature which make host plants attractive to insects. It is quite possible that the process of bacterial fermentation occurring in widely known yeasty baits results in the production of analogues of male pheromone components that function as aggregational pheromones.
The functional role of plant components in courtship behaviour of insects remains a disputable question. However, the chemical communications between higher plants and insects are varied and polyfunctional. Plants synthesise a great number of "secondary metabolites", substances the role of which in primary metabolism is unknown. As early as last century [see Isman, 1989], a hypothesis was offered that secondary plant metabolites may act as cues for plant recognition by insects or serve to defend plants from damage [Fraenkel, 1959; Thorsteinson, 1960]. By now about 20000 of such compounds have already been identified, and twice or thrice more are awaiting identification [Isman, 1989]. Male pheromone studies show that the same pyrrolizidine alkaloids in plants as well as their derivatives in the insect organism, can attract some insects and repel others [Boppre, 1990].
In view of the fact that the search for plants by insects involves their behavioural events (orientation, landing and assessment), more volatile plant substances are usually divided into attractants, arrestants and repellents, whereas less volatiles into stimulants and deterrents [Renwick, 1989]. The latter stimulates a certain behaviour type of insects or just retains them near the plant after alighting and coming into contact with chemoreceptors.
Volatile substances clearly permit an insect to learn the systematic position of a plant and determine its usefulness as a host plant for itself and its offspring, i.e. for egg laying. There is hardly any doubt that some organs of a plant, especially generative ones, also have specific chemicals facilitating the choice of landing place for insects. For a number of Lepidoptera, e.g. noctuids and tortricids, not only food attractants but also compounds stimulating egg laying have been identified [Renwick, 1989].
From the data available it can be concluded that the pheromone composition in Lepidoptera and, possibly, other phytophagous insects is determined by the chemical composition of host plants. The number of biochemical changes in the biosynthesis chain may vary with species. Since pheromone biosynthesis tends to simplify the chemical structure of a precursor [Bjostad et al., 1987], here we may have the rule: the more simplified the chemical structure of a pheromone, the longer the chain of its biosynthesis from a plant precursor and the wider the distribution and richer the behaviour functions of the pheromone components. And the second rule is: the rarer a plant precursor, the shorter the chain of pheromone biosynthesis and the more specialised the pheromone function. The latter is based on the studies of male pheromone origin.
Thus the chemical relationship between insects and host plants seemed to have played an enormous role in the development of pheromone system in Lepidoptera. Initially, insect ancestors seemed to have had only the system of perception of chemical signals emitted by plants. Later, when insects began to use plant components and their derivatives in inter- and intraspecific communication and defence from enemies, specialised glands and organs developed for accumulation and transmission of signal substances. In some insect groups the evolution of chemical communication system had, probably, stopped at an early stage. That is why in some insects, such as bark beetles, danaids and arctiids, a most close relationship is observed between pheromone composition and chemical composition of host plants. However, in many other insects, and particularly in most moths, this system kept evolving and by now has become independent of trophics. This may be considered proved at least for sex attractants of tortricid and noctuid females for which a significant correlation has been found between the chemical structure of pheromones and systematic position of species and higher taxa [Grichanov, 1991, 1993]. As things turned out, Lepidoptera have a most perfect genetic mechanism for this kind of evolution. For Trichoplusia ni, the genetic analysis showed that a mutation of only one autosomal gene is sufficient to cause a loss or addition of a new component in the pheromone system of a species [Haynes & Hunt, 1990].
As to the prospects of the use of male pheromones in plant protection, it can be concluded that the tasks usually solved in practice using female attractants (e.g. pest detection, pest population surveillance, and seasonal forecast of pest numbers and damage) can be set only for some arctiids, pyralids and agaristids, for which long-range female-by-male attraction is known. In Russia, there are pests among arctiids (Hyphantria cunea Drury and Arctia spectabilis Tausch.) and pyralids [Loxostege sticticalis (L.) and numerous secondary pests]. The above tasks are of promise for barn and flour pyralids, which have usually higher threshold densities indoors than other moths in agroecosystems. The conditions under which pheromones spread in a closed space are different from those in the nature. Therefore, short-range effect of sex attractants of some species is no problem for the practical use of products. For the above pest species, the attractive property of male pheromones can be used directly in pest control by means of mass removal trapping, sterilisation in traps and insecticide-attractant lures.
A fundamentally different approach to the use of male pheromones has been developed by H. Shorey co-workers [Hirai et al., 1978], based on the studies of the role of male pheromones in courtship behaviour in Pseudaletia unipuncta (Haw.). A hypothesis has been offered that biologically, the male pheromone serves to inhibit the activity of other males, thus eliminating competition for mate. Hence a possibility arises for artificial disruption of chemical communication of moths with their own weapons. Subsequently, K. Hirai  showed that benzaldehyde from glands of P. unipuncta males can well repel both sexually active males and females of P. separata Walker, Leucania loreyi Duponchel, L. striata Leech, Spodoptera litura (F.) and Etiella zinckenella Tr., and egg laying females of the last-named pyralid, as well as inhibit larval feeding behaviour of P. separata, S. litura and Mamestra brassica L.
It is quite possible that male pheromones from other moths can have still more surprising effect. Thus, these substances can, probably, be used to disrupt the chemical orientation of individual insects, with the same technology applied as in the case of sex attractants of females. They would, however, significantly differ in mode of action and in efficiency of equivalent doses of active ingredients. That means that as compared to the female sex attractant, a much lower dose of the synthetic male pheromone (non-specific in relation to individual, sex or even species) may be required to reduce a pest population.
Acknowledgements. The author thanks Prof. E.M. Shumakov, All-Russian Institute for Plant Protection, for valuable comments on the paper, and Miss G.A. Petrova for the translation of the manuscript. The work was supported by the Russian Foundation for Basic Research, Project No 97-04-49620.
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All-Russian Institute of Plant Protection
Laboratory for Phytosanitary Diagnostics and Forecasts
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